December 26, 2016 | Author: AlterMed | Category: N/A
MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
Native Wisteria (Millettia megasperma); Ellis Rowan watercolour, 1887 (Source: National Library of Australia).
MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
Cheryll J. Williams
ROSENBERG
First published in Australia in 2012 by Rosenberg Publishing Pty Ltd PO Box 6125, Dural Delivery Centre NSW 2158 Phone: 61 2 9654 1502 Fax: 61 2 9654 1338 Email:
[email protected] Web: www.rosenbergpub.com.au Copyright © Cheryll J. Williams 2012 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without the prior permission of the publisher in writing.
National Library of Australia Cataloguing-in-Publication entry Author: Williams, Cheryll. Title: Medicinal plants in Australia. Volume 3, Plants, potions and poisons / Cheryll Williams. Print ISBN: 9781921719165 (hbk.) Epdf ISBN: 9781925078077 Notes: Includes bibliographical references and index. Subjects: Medicinal plants--Australia. Materia medica, Vegetable--Australia. Dewey Number: 615.321
Printed in China by Everbest Printing Co Limited
Contents Foreword 7 Introduction: Toxic Plants – Friends or Foes? 8 1 Tales of Misadventure 15 Foraging Experiments 16 A Deceptive ‘Beach Bean 17 A Mangrove Poison 22 A Particularly Unpleasant Toxin 26 The Fearful Finger Cherry 31 Confusing Case Histories 35 Blue Lily Toxins 40 Stinging Tree Infamy 44 Medicinal Nettles 52 Table 1.1 Medicinal uses of Stinging Trees (genera Laportea and Dendrocnide) 55 2 Th e Art Of Detoxification: Refining Toxic Plants 60 Rainforest Blackbeans 61 Starch from Plants 64 Tacca: the Unique ‘Bat Plants’ 69 Table 2.1 Traditional medicinal uses of the Tacca genus 71 Riverine Rainforest Lianas 72 A Multipurpose Medicine 75 Wild Food: Foraging for Yams 79 Dioscorea: Yams of Distinction 85 A ‘Cheeky’ Yam 88 A Yam of Ancient Origins: Dioscorea alata 91 3 Convolvulaceae: Medicinal Bush Foods 95 Tubers from ‘Morning Glory’ Vines 96 New Research into an Ancient Crop 98 Bush Potatoes and ‘Underground Pumpkins’ 103 Pretty Purgatives 111 Table 3.1 Medicinal uses of Convolvulaceae herbs with acknowledged purgative attributes found in Australia 118 A Few Weedy Ipomoea 120
Magical Lianas: the Realm of the Mind 123 Table 3.2 Convolvulaceae species that contain ergoline alkaloids 125 Silver Morning Glory: A Valuable Traditional Medicine 125 Table 3.3 Medicinal use of the Elephant Creeper (Argyreia nervosa syn. A. speciosa, Convolvulus nervosus, C. speciosus) and related species 126 Ergot: A Remarkable Tale of a Poisonous Fungus 129 The Ergot Alkaloids 132 4 C ulinary Curiosities: Psychotic Potatoes and Tasty Tomatoes 136 Bush Tomato Tales 137 The Medicinal Tomato 142 Carotenoid Complexities 144 Tomato Antioxidants 145 Anticancer Carotenoids 146 Psychotic Potatoes 149 The Remedial Potato (Solanum tuberosum) 153 Glycoalkaloids: Poisons and Medicines 155 Gooseberry Goodies 158 A Herbal Panacea? 160 Table 4.1 Traditional uses of medicinal plants of the Physalis genus 163 A Medicinal Future 165 5 Aroids: Irritant Poisons 168 Hazardous Encounters with Native Aroids 171 Detoxifying Tubers for Food and Medicine 172 Medicinal Typhonium Tubers 173 Table 5.1 Summary of the traditional medicinal uses of Typhonium species 174 The Amorphophallus Yams 176 Konjac: A Large Tuber with a Big Commercial Future 179 Aroid Toxicology 182 The Oxalate Puzzle 183 Therapeutic ‘Elephant Ears’ 191
6 Caustics and Corrosives 198 Toxic Bush Tucker 200 The Anacardiaceae Family: Irritants and Allergens 202 Table 6.1 Common toxic trees of the Anacardiaceae that contain Urushiol components 205 The Indian Marking Nut (Semecarpus anacardium) 207 New Discoveries from a Traditional Medicinal Plant 210 An Anticancer Reputation 210 Cardiovascular Benefits 211 Pain-relief and Anti-inflammatory Effects 212 Cashew Nut oil: A Versatile Product 213 Anacardium: A Caustic Healing Agent 216 Table 6.2 Medicinal uses of the Cashew Tree with supportive investigations 219 Nutritional Nuts 222 The Mango Tree (Mangifera indica) 223 AnExtensive Medicinal Reputation 224 A Wound Healing Remedy 226 A Versatile Antimicrobial Agent 227 A Valuable Remedy for the Liver and Heart 229 7 Foaming Fish Poisons 234 Difficulties with Plant Identification 235 Bush Poisons 236 A Frothy Tale 239 Medicinal ‘Bush Soaps’ 245 Table 7.1 Medicinal Alphitonia 247 Fish Poison Wattles 248 Toxic Puzzles: Native Stock Poisons 252 Medicinal Albizia 258 The Siris Tree (Albizia lebbeck) 260 Deceptive Beauty: Fish Poison Trees 265 Myriad Medicinal Uses 267 Table 7.2 Investigations into the Barringtonia genus that support their traditional medicinal uses 271 8 Drugs From Ichthyotoxins 275 Poison Ropes and Wild Dynamite 276 Derris Insecticides 277 Rotenone from Lonchocarpus 280 Table 8.1 Medicinal Uses and Investigations of Derris and Lonchocarpus 282 The Genus Millettia: Native Wistaria 284 Native Tephrosia 289 Table 8.2 Medicinal uses of Tephrosia purpurea 292 The Poisonous Precatory Bean 295 A Bitter-sweet Medicine 296 The Abrin Toxin 299 The Fine Line between Toxin and Therapy 301 A New Order of Anticancer Drugs? 304 Murder and Mayhem: The Toxic Castor Oil Plant 305 Castor Oil: From Household Purge to Commercial Lubricant 308
A Popular Remedy for Skin Disorders 310 Table 8.3 Modern investigations into the Castor Oil plant 311 9 Poisonous Pteridophyta 314 Marsilea: A Toxic Water Fern 315 Medicinal Marsilea 320 A Mysterious Toxin 322 Medicinal Uses of Cheilanthes Ferns 323 The Bothersome Bracken 325 An Unaccommodating Neighbour 328 A Controversial Food Resource 329 Discovery of a Dietary Carcinogen 330 Cooking away Carcinogens? 333 Toxic Animal Fodder 338 A Medicinal Reputation 339 Table 9.1 Bracken as a medicament 341 A Toxic Anthelmintic 342 10 Cycads: Prehistoric Survivors 349 Table 10.1 Worldwide Distribution of Cycads 351 Unique Australian Cycads 351 Table 10.2 Major Australian Cycad species: Cycas, Macrozamia, Bowenia and Lepidozamia – location and conservation status 353 Strategies for Survival: Cycads and Insects 353 Persecution of an Ancient Plant 357 Ancient Survivors: Bowenia and Lepidozamia 360 The Genus Cycas 365 Cycad Seed Harvests 366 Starch from Cycads 370 An Unanticipated Toxin 370 Traditions from Antiquity 374 Macrozamia: Arrowroot Extraction 376 A Hazardous Crop 379 The Medicinal Side of Cycads 380 Cycads in Chinese Medicine 382 The Decorative Cycad 384 11 Neurotoxins: Plants of Perilous Consequence 385 Cycad Toxins 386 Intricacies of a Poisonous Puzzle 387 A Matter of Exposure 390 A Cyanobacterial Link 394 Toxins from the Sea 401 Dietary Neurotoxins 404 Prunus and Manihot: Cyanide Poisoning 410 Cyanide in Seeds: The Rosaceae 413 Resources 418 Index 461
Foreword Australia possesses a wonderland of the botanical world of mosses, ferns, fungi, algae, flowering plants and trees. The animal and plant kingdoms have evolved in concert. Animals have evolved and changed to exploit the flora of their environment. Many, including us, are dependant on it. Many plants have evolved to depend on animals for services as diverse as pollination and nutrition. Over the aeons, this congruent life has so often been one of tension – plants evolving protection and animals bypassing the arms and armour of plants. Over recent millennia plants have provided extensive drugs and medicaments for the benefit of all humankind. In the twenty-first century, some 60 per cent of all the drugs prescribed for human use are derived from the world of botany. With knowledge, humankind has enjoyed the dominant role in this nexus. Hunter-gatherer cultures learnt the secrets of medicinally useful and toxic plants by trial and error; and certainly by natural experiments. Throughout the world, men and woman have both benefited from and suffered because of (often with fatal consequences) such contact with plants, both accidental and deliberate. Every pre-literate indigenous culture in the world has developed a sophisticated and extensive knowledge of the medicinal and toxic properties of the flora of their range. The Aboriginal peoples of Australia, men and women who today comprise the world’s longest surviving culture, have held and continue to possess such a compendium of encyclopaedic botanical lore. Fragments of that lore have survived into the present. Some of that knowledge has been enjoined into mainstream pharmacobotany and toxinology. In this context, a poison is defined as any physical agent which, in small quantity, is injurious to metabolism or to tissues. A toxin is a poison which is manufactured by a living organism. Botanical
toxinology, as a documented science, dates from the time of ancient Greece and specifically from the writings of Aristotle in the third century BC. Since that time, documentation by zoologists and botanists and knowledge accumulated by planned and accidental experimentation continues today. The result is a compendium of knowledge that comprises the botanical pharmacopeia of Australia. In Australia, much has been gained by a fusion of this enduring Aboriginal lore and by scientific study over the last two centuries. Much of the knowledge of the medicinal and toxic properties of Australian biota has been contributed by scientists or clinicians who treated victims of poisoning. Much has been learned also from the unpaid contributions of naturalists, farmers, agriculturists and hobbyists. Much still remains to be learnt. Botanical species which affect metabolism and the integrity of mammalian tissue can be both beneficial and destructive. The outcome from such contact is often dose-dependent. This book summarises the essential knowledge of eleven different themes which are germane to this subject – themes that range from the dangers of eating toxic ferns to the historical use of fish poisons. Sixty per cent of Australians identify gardening as their favourite outdoor hobby, often one which is passionately held. Many others delight in bushwalking and camping. Some of us have an enduring interest in the bush and the rainforest; and delight in the individual species of tree, herb, fern and fungus and their enormous diversity. This book is for all who have such an interest or wish to learn more about this nexus which will protect us from injury or harm, or death. Such knowledge will empower the reader to both respect the power of medicinal and toxic plants on the one hand – yet on the other be protected from their potential harmful effects.
Professor John Pearn AO RFD MD PhD DSc Fellow of the Linnaean Society Sometime Medical Member, The Queensland Pollen and Plants Committee Royal Children’s Hospital, Brisbane, Australia 2012 7
Introduction
Toxic Plants – Friends or Foes? The adventure and challenge of the Australian flora is, in many ways, unique. The plant lineages of this ancient land originate in a past that goes beyond human imagination. There are innumerable floral innovations, developed over millennia, that continue to have an indisputable role to play in the modern world. Those plants that are useful to man are diverse. Some are weeds, some are immigrants from ancient times, and some evolved here. All, importantly, illustrate the value of these plants over the ages – whether they provided herbal remedies, culinary resources, innovative commercial enterprises, or inspired drug developments. However, this rich floral diversity often poses challenges to those who would extract its secrets. The idea of exposure to toxic plants, for the majority of us, is directly associated with worries concerning our mortality. Encounters generally conjure up images of extreme discomfort (at the very least), with advancing degrees of debility, pain, and the looming spectre of an untimely demise. Even so, the hazards of toxic plants would appear to be over-rated in comparison the distress caused by viral, bacterial and parasitic infections – which have the potential to be far more hazardous, with potent debilitating consequences and, at times, high mortality rates. This does not belittle the clever chemical defences that plants have utilised in a world where they are struggling to live and propagate to ensure their species survival. It just means that plant toxicology is but one aspect of the perilous challenges that humans face, and this needs to be put into perspective. Humanity’s survival is linked to reliable food procurement skills. This imperative would have led to encounters with poisonous plants since time immemorial – and to the first experiments in devising detoxification processes. In this respect toxic plants represent far more than poisonous puzzles for the
While most of us would view poisonous plants as being responsible for serious illness, in reality this is a relatively uncommon occurrence. Children tend to be at the forefront of these experiences through their curiosity and willingness to experiment in an unexplored world. In this respect, it is extremely surprising to find that innumerable house and garden plants rate toxicological concern, particularly aroids. These contain calcium oxalate crystals that cause irritation of the oral mucosa, as well as gastroenteritis – albeit usually of a mild nature. Peace Lilies, Philodendrons and Poinsettia are among the most common culprits (Petersen 2011). Unfortunately, it is often overlooked that common household cleaning products and pesticides present a far more dangerous risk.
toxicologist to solve. They have been one of the greatest challenges to human survival on the planet. They deploy a wide variety of defences. There are those 8
Toxic Plants – Friends or Foes?
that advertise their intent with obvious deterrents such as stinging hairs, or a caustic, irritant latex. Fruits or tubers often utilise extremely bitter and unappealing taste sensations. However, there are other food resources that were more deceptive. Without the knowledge of precise harvesting or processing skills, experimentation with them could easily result in a great deal of discomfort. This was usually linked to gastrointestinal distress such as purgation or emesis. On occasion, the consequences were far more drastic. Even so, taming many of these plants was to provide a source of sustenance that has resulted in many indispensable foodstuffs, some of which form the basis of multi-billion dollar commercial enterprises today. Most of us take little time to consider the origins of our food resources – we have little need to. Even fewer would appreciate the developments in plant breeding that have led to the remarkable array of fruits and vegetables that now grace the supermarket
Port Douglas markets: concerns about food additives have made home produce stalls at local markets increasingly popular. Despite all the advances in food technology, serious dietary-induced disorders continue to exist that provide cautionary examples of the potency of food items. This is an essential part of our relationship with the environment that is often relegated to the unexciting by the medical profession. Yet to find and diagnose food intolerances or allergic reactions can be among the most challenging aspects of medicine. These are complex problems. Treatments that rely on anti-inflammatory or steroidal drugs, albeit often a solution to the immediate crisis, do not deal with the origin of the disorder. This can leave the sufferer to run the risk of continued exposure and long-term damage from repeated insults that can seriously compromise the immune system. In many cases, the addition of food additives (preservatives, colourings, sugars, emulsifiers, etc.) to the diet compounds the situation. Diagnosis is problematic at best and, in some cases, almost impossible. (Image courtesy: Tony J.Young)
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shelves. Indeed, the centuries of exploration and discovery that resulted in the marketable produce we see every day is simply astounding. This journey of discovery continues. In Australia, the native food industry has excellent potential to yield raw materials for the innovative development of modern-day crops. The use of a great diversity of floral resources could never have happened without the discovery of some rather innovative food-processing strategies. Indeed, the ability to utilise plants with potentially poisonous dietary consequences has been linked to the development of traditional culinary techniques. While we do not know where and how they originated, those in common practice in Asia migrated to this continent with the first Aboriginal inhabitants. They were, however, unfamiliar to the early European immigrants and unfortunately, because of this, these traditions were often considered to be little more than a curiosity. A few explorers realised that they needed to be discerning with regard to their use of local resources. Survival in many parts of the continent pitted them against a harsh and highly inhospitable landscape. Little was familiar. The writings of Ludwig Leichhardt are full of interesting observations in this regard. During his travels in 1847, he astutely surmised that detoxification of certain seeds and nuts was a necessary prerequisite for their use as a food resource: The natives, at this season, seemed to live principally on the seeds of Pandanus spiralis and Cycas, but both evidently required much preparation to destroy their deleterious properties. At the deserted camp of the natives, which I visited yesterday, I saw half of a cone of the Pandanus covered up in hot ashes, large vessels (koolimans) were filled with water, in which roasted seedvessels were soaking; seed-vessels which had been soaked were roasting on the coals, and large quantities of them broken on stones and deprived of their seeds. This seems to show that, in preparing the fruit, when ripe for use, it is first baked in hot ashes, then soaked in water to obtain the sweet substance contained between its fibres, after which it is put on the coals and roasted to render it brittle when it is broken to obtain the kernels.
The dangers inherent in some harvests from the Australian flora could have severe consequences for the unwary, and incidents of poisoning became well advertised warnings for the populace. Dr George Bennett recounted a disturbing story with regard to
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
poisoning by ‘fern nuts’, entitled ‘On Macrozamia spiralis, or Burrawang of New South Wales’, and published in the New South Wales Medical Gazette of October 1871: A little girl, 3½ years of age … was accidentally poisoned on Friday last, by eating a species of fern nut, a number of which had been brought into town from the country a few days previously. Mr. Morrison, being unaware of their highly poisonous properties, gave them to his children to amuse themselves with by playing ‘knuckle-bows’. A short time afterwards he observed that his little girl … had eaten one of the nuts, which present a very inviting appearance to any person unacquainted with them. She was suddenly taken very ill – violent vomiting, stupor, and a yellowish appearance of the eyes, being amongst the most noticeable symptoms of her malady. She remained in a state of stupor until yesterday, when she commenced slowly to recover, and from the latest inquiry we are glad to state she is going on favourably towards recovery … These nuts are found in the pineapple-shaped pod which grows on the ordinary fern. The pod, which is green inside and red outside, is formed in a precisely similar manner to the pineapple, being made up of layers, inside of which the nuts are found. It is said the aboriginals eat them after the narcotic poison they contain has by some secret process been extracted.
Plants with poisonous potential have attracted interest for other reasons. The deployment of fish poisons (piscicides or ichthyotoxins) involved experiments with diverse products that simplified the art of catching fish. These plants were among the most obvious choices for toxicological evaluation. Professor Geoffrey Blainey commented on this subject in a 1977 article on the early Australian pharmacists: How many varieties of bark, leaves, vines and roots were used to poison will never be known, but probably there were many. In the rivers flowing into the Gulf of Carpentaria the coolibah or flooded box tree [Eucalyptus microtheca] grew up to 30 feet high and its leaves or bark were pounded and then immersed in the ponds in the hope of stupefying fish. Near Geelong the bark of a willow was used, while small lagoons and waterholes of the Cloncurry River were poisoned with the tiny pods and thin leaves of the Tephrosia, a small bluish shrub. In some parts of Queensland a poisonous bark was placed in a dilly bag, which was lowered into the creeks – like a Tetley tea bag.
Cycad fruits are highly toxic and require specialised preparation. The methods designed to do this originated in a lost past. A comprehensive review of the topic by JM Beaton (1982) in Fire and Water: Aspects of Australian Aboriginal Management of Cycads emphasised the fact that detoxification was essential to their use for food: ‘Cycads were likely not among the first plants leached by man … They are too unforgiving. By the time the leaching technology was applied to cycads it must have already gone through its experimental stages on other, less offensive plants. The technology must be kept well oiled and fine-tuned if cycads are to be processed. Whatever else they might mean to man, cycads are a danger.’ It is only today that we have truly begun to appreciate the great depths of that danger.
Joseph Maiden provided a brief list of these fish poisons, commenting: ‘It must not for a moment be supposed that it includes even a small percentage of our indigenous poisonous plants, scores of which could be at once quoted as being undoubtedly deleterious to fish’. This appraisal led him to suggest, ‘Nevertheless it would be interesting to take even the few I have quoted, subject them to chemical analysis, and thus decide to what substance the effect first noticed by the aborigines on fish is due’ (Maiden 1895). The challenge was taken up by later investigators – who made some very interesting discoveries. The fact that, over the centuries, Aboriginal people had extensively experimented with the native flora went largely unappreciated by the majority of the early colonists. This lack of regard was compounded by some rather fabulous tales that surrounded native medical practices. A superstitious fear of these perceived ‘magic’ practices and ‘sorcery’ arose – circumstances
Toxic Plants – Friends or Foes?
that readily lead to misconceptions. A mutual lack of comprehension and appreciation of the culture of either race did absolutely nothing to help matters. In The Enchanted Herb: The Work of Early Medical Botanists in Australia, Professor John Pearn (1987) pays tribute to the practical knowledge of the Aboriginal people: ‘Of course the Aboriginal pharmacopoeia had been highly developed millennia before the First Fleet. The country’s original inhabitants were superb botanists, sophisticated pharmacognosists of the indigenous flora, and were well aware of and exploited the phenomenon of pharmacological variation among different races of the same species of plant.’ This posed complex problems. Unravelling the pharmacology of the native plants was not going to be an easy task for the early scientists. In particular, chemical variation (even within a single species) ensured that some plants, and not others, showed good activity. Some samples could even be chemically inert. Even today, this type
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of puzzle plagues chemists dealing in natural product research. Aside from the culinary importance of the native flora, poisonous plants were of considerable concern for farmers and graziers. The scientists involved had to deal with complex chemical puzzles that involved a steep learning curve and a need for innovative solutions. Stock toxins were a particularly challenging subject and a lot of information regarding the poisonous potential of the native flora came from these sources. It is interesting to find that plants as a drug resource provided an important impetus for their study in Australia. The fact that toxic plants can have serious medicinal value should not come as a surprise – such knowledge dates back to the great physicians of antiquity. Plants with substantial toxic potential have always attracted special attention from the medical world. Numerous drugs have been developed from this starting point. This was linked to the fact that,
Hemlock (Conium maculatum) The infamous Hemlock is one of the weedy Australian imports that aptly illustrates the serious potency of some toxins. The herb is fairly widespread along the east coast, ranging from southern Queensland, New South Wales and Victoria, to South Australia and Tasmania. It gained a level of notoriety in ancient Greece as an executioners’ poison – which was the instrument of Socrates’ demise when he was deemed guilty of the crime of impiety in 399 BC. The herb’s notorious reputation has occasionally resurfaced down the ages. A more recent report of Hemlock poisonings by Olaf H Drummer and colleagues, published in the Medical Journal of Australia in 1995, recounted a couple of more localised incidents. A couple of men, having a social New Years’ evening together, undertook a rather foolish and uninformed venture that led to their rather untimely demise: ‘Both had consumed large amounts of alcohol the previous night. They were observed going out after midnight and returning an hour later carrying a quantity of green vegetable matter. They were seen boiling this leaf matter in a pot full of water, and then were not seen from
about 2.30 am until their discovery at 10.00 am.’ The authors concluded that: ‘While the symptoms of the two deceased men were not known, it is likely that narcosis occurred, followed by collapse of the cardiovascular system. The concomitant presence of ethanol in medium to high concentrations would undoubtedly have contributed to the depressant actions of hemlock alkaloids. It would also appear from the circumstances that the two men knew of some “drug-like” properties of this plant.’ Another incident involved a 3-yearold boy who ate some leaf material and appeared to go to sleep in the car seat. Two hours later he was found dead. Hemlock contains a group of toxic alkaloids (coniine, conhydrine and their derivatives) that are present throughout the plant. They are particularly prevalent in the flowers and fruit, with lesser quantities found in the roots. The leaves, before flowering, contain the most alkaloids (Cooper & Johnson 1984). While records note that coniine is destroyed by drying and heat, this cannot be guaranteed – as the previous tale illustrates.
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
Tomorrow the Forest, original artwork by Peter Brooke. The secrets of the Australian flora are diverse and remain a mystery, full of chemical intrigue for the future.
for a long time, alkaloids were the main driving force for drug research. These compounds were relatively easily detected and testing systems were developed that could, fairly easily, follow up on this type of chemical lead. It was also a profitable enterprise. This search led to the discovery of a number of exotic drug plants (and their active chemical components) that included Strychnos spp. (strychnine) from Asia and Africa, the Ordeal Bean Physostigma venenosum (physostigmine) from West Africa, Chondrodendron tomentosum (curare) and Pilocarpus jaborandi (pilocarpine) from South America. These drugs have played an indispensable role in surgical procedures and ophthalmology. Today much of our past reliance on food and medicinal plants lies unappreciated. While this is slowly changing, the traditional wisdom regarding their practical use has often been simply consigned to obscurity. It is fitting that the value of medicinal plants, in particular, should be re-appreciated as they form the basis for numerous developments upon which
modern medicine has been built. Some rather amazing advances have come from these origins. Piscicides have yielded a range of insecticidal compounds, some of which are still in use in the garden. Later, drugs with a profound effect on neurological function were developed. A fairly common example of a useful poisonous plant is Ricinus communis, which contains a potent neurotoxin – as well as being the source of castor oil, that much-dreaded, nauseating scourge of childhood in earlier times. This plant, which is found as a weed throughout the Australian continent, has played a major role in natural product developments that range from pharmaceutical drugs, cosmetics and toiletries, to engine oils and biowarfare agents. While many native plants have toxic reputations, in a large number of instances there is little idea of whether they have any other potential. It is time that this changed. Indeed, many of the mysteries regarding the chemistry of the native flora are unlikely to be unravelled without a great deal more investigation. The story of past advances in toxicology serves to
Toxic Plants – Friends or Foes?
illustrate some rather remarkable scientific and medicinal achievement – as well as pointing the way to an interesting phytochemical future.
Author’s Acknowledgments
The feast of images presented here are the result of many hours of painstaking work. The search for the majority has fallen to Tony Young who, with his normal determination, diligence and great patience, ferreted out many that I do not have in my files. Within this category are included a number of older drawings by botanical artists – to whom we owe a great debt of gratitude for their beautiful and accurate floral artistry. In many instances, their meticulous representations of individual plant species are as valuable now as they were when they were first executed. As this is a private venture, funding constraints mean that we are totally reliant on the goodwill of the individuals whom we contact for images – and we have been very fortunate that those who felt unable to assist were few. The ever-generous contributions of Forest and Kim Starr from Hawaii, Peter Woodard, Brian Walters and the Australian Native Plants Society (ANPS) have been a mainstay of some sections. As usual, we had difficulty finding images of some of the more obscure Australian plants and, although a few were unobtainable, we have been extremely lucky in securing help from the University of Western Australia, the WA Department of Agriculture and the WA Herbarium, as well as the State Herbarium of South Australia. The botanical expertise of Brendan Lepschi (Australian National Herbarium) has, once again, been invaluable for resolving the intricacies of botanical classification. Support for the identification of plant images has been provided by David Warmington, Andrew Small, Peter Newell and Bob Jaygo. There are a few special people who have contributed significantly toward making this volume a reality. The excellent research skills of Brigitta Flick and Tony Young have been instrumental in ensuring the technical integrity of this work. The proofreading capabilities of Tony and Helen Timms have also been exceptional, as have the editorial contributions of Anne Savage.
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As always, we have tried to track down those who contributed so generously to Wikipedia – a remarkably wonderful and visionary resource. To those of you whom we were unable to contact personally we would express our heartfelt thanks for your generosity. In addition, there were many companies and individuals who willingly supplied their work and went to the trouble to send high resolution images. They were always a delight to receive. A special thank you is due here to JM Garg in India. While we have tried to obtain most product images from Australian companies, unfortunately, there have been times when this was simply not possible. On a personal note I would like to express a heartfelt thank you to Gloria Schlotterbeck for her unwavering faith in my abilities (and constant nagging), which helped to make this work a reality. Peter Brook gets a special mention for not being too tired to listen when I was trying to unravel the intricacies of medicinal plants – and for helping to make the tedious job of chopping mountains of fruit for the animals in care just that little bit more sociable. Dr Sue Cory has been another mainstay in helping me stay well enough to pursue this venture, and deserves my deepest gratitude for her untiring efforts. Appreciation for their continued faith in this project must also go to Chris Crosland, Jenny Sheppard, Margaret Lee, Lolli Forden, Bruce Allen, Ian Mackay, Jill Richardson, Kathryn Collis, Sue Jordan, and Barbara and David Leigh. In addition, I must mention a few important individuals who provided substantial support at the inception of this work: Valerie Beggs, Paul Coxon, Nick Christopher, Steve Goodman, and Caroline and Graham Wood. I would also like to thank Margaret and Frank Young, without whose support I would not have had the wonderful opportunity to enjoy the feast of knowledge on medicinal plants housed within the British Library – and would probably have never been able to afford to set out upon this publishing venture. This book is also a timely publication on the advent of my mother’s 80th birthday – when she flew off to Sydney and walked over the top of the Harbour Bridge.
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
Barringtonia asiatica is known as the Beach Barringtonia or Fish Poison Tree. It is among the most impressive of the native coastal vegetation, with stunning filamentous blossoms.
Chapter 1
TALES OF MISADVENTURE
When the early colonists arrived on Australian shores little of the flora was familiar to them. The desire to quickly acquire food resources was driven by an urgent need and, therefore, the role of the botanist was far more essential to the success of the venture than we would appreciate today. Some experiments with the local flora were fortuitous, finding luscious looking fruits that were, at least sometimes, palatable. However, food plants on the Australian continent had not undergone the refinement of centuries of cultivation, as had occurred with many European and Asian resources. Discovering local substitutes for ‘greens’ and root vegetables was an essential part of establishing a colony. Medicinal herbs were, of course, another priority. Fruit trees were equally desirable, although there were a few native plants that would suffice as substitutes. Plants can be masters of deception and the Australian flora was to provide many examples of strategies that were not designed to entice man to act as a seed dispersal agent. For instance, numerous rainforest fruits, which have an unappealing flavour for humans, would be designed to attract a different animal distributor, particularly bandicoots, possums and rodents. There are a number of other native fruits that, despite their inviting appearance, defend themselves with poisons – while others may yield luscious-looking fruit that is simply inedible. Over time, through trial and error, their usefulness or toxicity became familiar. The knowledge of the plants with harmful potential, as well as those that were unpalatable, was passed down through generations of Aboriginal inhabitants. Even so, the risk of serious poisoning always awaited the unwary – or those who would not heed the advice of their elders. Although
The cassowary (Casuarius casuarius johnsonii) is an example of a major seed distributor of the northern rainforests – a big bird with a system that can allow toxic seeds to pass though unharmed, and essentially bury them in a pile of poo fertiliser. In this way the forest trees expand their territory and regenerate in an exceptionally challenging environment.
not all experiences were disastrous, fatalities did occur. Many fruits provide a warning of their toxic intent by having disruptive consequences for the digestive system. This not only involves gastric upset – merely tasting some plants can cause an immediate aversion due to an unpleasant flavour. The green fruit of the Solanaceae family provide a perfect example. They usually contain toxic glycoalkaloids, particularly the genus Solanum, which is widespread throughout the Australian continent. While the fruit generally lose their poisonous qualities as they ripen, this is not true for all native species. Some will retain their toxic character. There are other resources with a highly variable character – as is the case with the native yams 15
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
(Dioscorea spp.), some of which were palatable and others definitely not. Other food resources such as the Blackbean (Castanospermum australe) and Cunjevoi (Alocasia macrorrhiza), while not considered a first rate choice, could be made fit for the table. However, the detoxification strategies were quite laborious. It could take a lot of processing and time before the result was deemed edible. Even so, some plants would only ever yield foodstuffs considered to be a form of ‘famine food’, merely fit for times of desperation. Vegetable or fruit resources that were regarded as being fairly tasty were more relatively uncommon and often less accessible. In addition, there were some plant resources
that were scrupulously avoided. Those that were considered to be strictly ‘off limits’ frequently had highly irritant potential. Some contained a caustic sap with extremely unpleasant effects on the skin or eyes. They included the Milky Mangrove (or Blindyour-eye, Excoecaria agallocha) and the Native Cashew or Tar Tree (Semecarpus australiensis). Contact with the latex can result in extremely painful blistering – a sure hint that the tree should be left alone. Sometimes, experimentation incurred adverse effects with dramatic, and irrevocable, results. Eating the fruit of the Finger Cherry (Rhodomyrtus macrocarpa) could have particularly disastrous consequences that resulted in blindness. This was often permanent, with no known cure.
Foraging Experiments
The Blackbean (Castanospermum australe) is an impressive tree that can grow to massive proportions in the rainforest. It produces woody pods that contain large chocolatecoloured seeds. Aboriginal people harvested the ripe seeds from underneath the tree from May onwards. They require complex processing, an art at which the women of the tribe were particularly adept. Ultimately a flour was produced that could be used to prepare cakes and dampers.
Cycas media in riverine habitat.
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The accumulation of accurate information regarding poisonous plants in Australia was to prove to be a difficult task, with practical experiences that often provided some very harsh lessons. From the time of the first explorers the toxic potential of the vegetation was quickly appreciated. Selwyn Everist (1964) provided an outline of the problems involved in determining the floral culprits, with particular reference to forage for livestock: The first recorded feeding test of a suspected poisonous plant in Australia was carried out at the Endeavour River in 1770, when seeds of a cycad, probably Cycas media, were found to be toxic to pigs … By experience, early explorers and settlers found out that many of the native plants were toxic to their live-stock but often they were unable to identify the particular plants responsible. Some information on the properties of the native plants was gathered from the aborigines but communication with these people was poor and they had no experience in the husbandry of large flocks of ruminants. The native grasseaters were marsupials, not under close control and, as we have since discovered, often not affected in the same
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way by some of the native toxic plants. Therefore, the European settlers had to rely on their own experience. Local knowledge of poisonous plants grew slowly … communication between graziers, stockmen and drovers was slow, restricted in scope, often very localized and rather haphazard. This local experience was of little value until it could be collected and properly organized. The first step in the organization of this knowledge and experience was accurate identification of the plants themselves, the recognition, naming and description of the plants which grew in the new continent. From the time of Banks and Solander, who accompanied Captain Cook in the voyage of 1770, explorers, botanists and others were active in collecting plants.
The collation of botanical information by George Bentham, which resulted in the publication of the multivolume Flora Australiensis between 1863 and 1878, did a great deal to resolve this situation. In 1942, Evelyn Hurst’s The Poison Plants of New South Wales provided another invaluable reference. This was eventually followed by an impressive tome in 1981 entitled The Poisonous Plants of Australia by Selwyn Everist.
A Deceptive ‘Beach Bean’
The Canavalia genus contains around 48 species of legumes that can be found throughout the world’s tropical regions. Five species are found on Australian shores. Canavalia rosea (C. obtusifolia or C. maritima in the older literature) is found distributed along much of the Australian coast – from New South Wales to the northern tropics (Queensland, Northern Territory, Western Australia).
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
The toxic Mackenzie Bean (C. papuana), which was responsible for poisoning on Ludwig Leichhardt’s expedition, has been discussed in Volume 1. The Horse, Sword or Jack Bean (C. ensiformis), which has become naturalised around the world, is only found in Western Australia. The Mangrove Bean (C. cathartica) has a somewhat wider range across Cape York, and the islands off the Northern Territory – as well as extending its range to India, Malesia, and the Pacific Islands.
The pink-flowered Beach Bean, Canavalia rosea (syn. C. maritima) is an attractive viney coastal plant with distinctive pods that resemble the Broad-bean. Henry Burkill mentioned that in Malaysia the young seeds ‘make a good pease porridge, not uncommonly eaten. The pods are edible when young’ (Burkill 1935). The native species appeared to be identical to the Asian plant and, when in Indonesia, James Cook had tried the dish. This led to experiments at the Endeavour River in northern Queensland. Therefore the bean naturally attracted the notice of other settlers in the early days of colonisation. However, there were some technicalities involved in their collection and preparation – and not all species could be considered equally palatable. There are records of some initial experiences that quickly advised caution in their use. In 1770 SurgeonGeneral John White provided a clear account of his encounter with the plant: As we proceeded along a sandy beach, we gathered some beans, which grew on a small creeping substance not unlike a vine. They were well tasted, and very similar to the English long-pod bean. At the place where we halted, we had them boiled and we all eat very heartily of them. Half an hour later, the governor and I were seized with a violent vomiting. We drank warm water, which, carrying the load freely from our stomachs, gave us immediate relief. Two other gentlemen of the party ate as freely of them as we had done, without feeling the smallest inconvenience or bad effect.
The Silky Jackbean, Canavalia sericea, is found along the central Queensland coast, and throughout the Pacific Islands, including Hawaii. It is a beach species that has been used as a cover plant in Cocos plantations in Polynesia. (Images courtesy: Tau’olunga, Wikipedia, plant; Kim and Forest Starr, Hawaii, leaves)
It is possible that the discrepancy in their experiences could be linked to some of the party sampling the beans raw, in which state they can be quite toxic (Low 1992). Certainly, in some parts of Australia, Aboriginal people did not consider the Beach Bean edible, although in other areas they were cooked and made into cakes. Queensland pastoralist Tom Petrie mentioned the use of Canavalia obtusifolia (C. rosea), which was harvested before being completely ripe. The beans were soaked in water, pounded up and made into cakes: ‘The natives declared that the soaking and roasting took all badness away’ (Petrie 1904). The roots were also regarded as being medicinal in Broome, Western Australia where an infusion was applied locally for aches and pains, rheumatism, leprosy and for treating colds (Webb 1969).
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be used with great caution. These are pink-flowered, and seeds are usually of a curious bright pink. The writer has known of a dog being made seriously ill by eating them, not raw, but cooked.
Canavalia: Medicine Beans
It is interesting to find that there are widespread reports from South America, the Gulf Coast of Mexico, and Africa, of the beans of Canavalia maritima being eaten or smoked with dried leaves as a ‘marijuana-like’ drug. An active principle (L-betonicine) has been isolated from the plant, which is suspected to be similar to that found in marijuana, although there is no conclusive proof of its effect (Seena & Sridhar 2006).
Len Webb mentioned that the seeds of the Sword Bean (Canavalia gladiata) ‘were reputed poisonous if inadequately cooked and to have medicinal uses by Chinese living in north Queensland’ (Webb 1948). Indeed, Selwyn Everist (1981) commented that the seeds of most species of Canavalia contained cyanide (HCN) when mature, although the immature beans could be cooked and eaten like ordinary beans. It would, however, appear that some species were less toxic than others. Henry Burkill observed that the young flat pods of Canavalia ensiformis (syn. C. gladiata) could be: sliced, cooked and eaten with impunity, or even eaten raw. In Java the ripe seeds eaten also but only after adequate boiling with salt; and both the flowers and young leaves steamed and used as flavouring. But any inferior race must
Canavalia gladiata. The seed, root, and pod shell of this white-flowered species have all been utilised medicinally. (Courtesy: I Kenpei, Wikipedia, CCASA 3.0)
The Sword Bean (Canavalia gladiata), although not widely valued as a medicinal plant, has been used therapeutically among the Chinese. The Reverend GA Stuart (1911) summarised its usefulness: ‘They are much relished as an article of diet by the Chinese; the pods, while still tender, being fried and eaten with soy or honey, and the beans, when ripe, being cooked with pork or chicken. They are thought to benefit digestion, to strengthen the kidneys and to be constructive and tonic. They are especially recommended in cases of weak digestion during convalescence from acute disease.’ In addition, the shell and root were used
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as a detoxicant (‘clears the blood’), the shell provided an antidiarrhoeal remedy, while the root was also employed as an analgesic (Chang 1989). There are a few interesting recipes based on its use. The root decoction was particularly useful for treating lumbago with kidney pain (simmered roots cooked with glutinous rice), or lumbago with rheumatism (the root simmered in wine and water). The cooked seeds were also recommended for lumbago with kidney pain (chewed with a little wine), and for treating hernia in small children (powdered seeds taken in water). For lumbago during pregnancy the shells were utilised (a soup made from bean shells and an egg); and for hiccough (roasted shells made into charcoal and powdered; taken with warm water) (Chang 1989). Henry Burkill mentioned in the Medical Book of Malayan Medicine that the leaves were used with other substances in a kind of magic tonic squeezed into the eyes, and that the pounded plant was a useful treatment for boils (Burkill 1935). Unsurprisingly, in Asia, Malaysia and Indonesia it was recognised that, despite cooking, there could still be a risk of poisoning with some Canavalia species. This led to some extra precautions during processing. In Vegetables of the Dutch East Indies (1931) Dr JJ Ochse described a rather elaborate process that accompanied the use of Canavalia gladiata: This plant has narcotic properties. The large seeds are eaten as dage, but only after they have been thoroughly prepared. Otherwise they are positively poisonous! In order to prepare dage of these beans they are twice cooked during a long time; the water is renewed after the first time. The second time the beans are cooked till they have become quite soft. Then they are washed in fresh water, deprived of the testa and soaked during two days in floating water … Next they are covered with banana-leaves and left to ferment in a cool place during 3–4 days.
Only then, once they were re-cooked, were they considered edible. Henry Burkill also observed that in one or more races the seeds were brown, and these were ‘apparently as much to be avoided as the pink-seeded plants’.
Mangrove Legumes
Canavalia cathartica. From Manuel Blanco 1880–83, Flora de Filipinas.
The Mangrove Bean (Canavalia cathartica) is a coastal species that has been utilised in India and Asia for dune stabilisation works. The roots were employed medicinally in India for treating skin disorders (Seena & Sridhar 2006). A number of studies have undertaken evaluations of this plant, as well as the Sword Bean (C. gladiata), Jack Bean (C. ensiformis), and Beach Bean (C. rosea syn. C. maritima) – demonstrating their high quality protein values. The level in Sword Beans (around 28–32%) is higher than most legumes. Those of the Jack Bean (25–27%) and Beach Bean (C. rosea: 27%) are similar. The fat content is low, albeit valuable due to its unsaturated fatty acid content (linoleic and linolenic acids). There is a high level of potassium, and good amounts of vitamin C, vitamin A, calcium and iron – although, overall, additional mineral fortification would be desirable (Doss 2011; Akingbade 2009; D-Cunha 2009; Bhagya 2006; Seena 2006; Seena & Sridhar 2006; Sridar & Seena 2006; Ekanayake 2000).
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There is a paucity of investigations examining the pharmacological potential of the Canavalia genus, although a few studies are of interest. The phenolic content of C. gladiata and C. ensiformis seed flours (221.3 and 245.5 mg/100 g, respectively) contained flavonoids as the main components of interest, the levels of which were higher in C. gladiata (48.15 mg/100 g) than in C. ensiformis (29.3 mg/100 g). This would account for the potent antioxidant (radical scavenging) effect of the Sword Bean extract (Doss 2010). Seed proteins have shown cholesterol lowering and hypoglycaemic activity. Alpha-mannosidase from this species also demonstrated immune stimulant properties. A fermented seed solution from C. gladiata has shown anticancer activity, significantly reducing the viability of liver cancer cells. The amino acid canavanine, which has anticancer properties, has been employed in pancreatic cancer studies. In addition, an extract of C. cathartica acted on the central nervous system, potentiating the sedative effects of some drugs (pentobarbitone, morphine) (Sridhar & Seena 2006). Canavalia beans are well known to contain anti-nutritional factors, that is, components that compromise their nutritional value, some of which are toxic. The most interest has centred around lectins, notably concanavalin A (Con A, phytohaemagglutinin) which has significant haemagglutinin activity – in other words, it initiates the blood cell agglutination that results in clotting. While the presence of this lectin is not a desirable attribute for a food product, it is particularly useful for biochemical studies – notably the determination of blood groups and for the isolation of substances such as immunoglobulins or glycoprotein hormones. In addition, Con A is of interest for its antiviral, immunomodulatory and mitogenic properties. It has been utilised as an important cellular binding agent in neurological studies, tumour diagnosis and therapy. In the digestive tract Con A binds to carbohydrates in the intestine and retards the digestive process. However, this is fairly easily solved as roasting and pressure-cooking reduces its activity (Seena 2006; Sridhar & Seena 2006). Other anti-nutritional factors include a neurotoxic protein (canatoxin1), as well as tannins (polyphenols) Canavalia cathartica (flowering vine and pods). (Courtesy: Kim and Forest Starr, Hawaii)
1 Canatoxin is not uncommonly found in legumes, although it is not present in peanuts and castor oil seeds. Experimentally, it is highly toxic when given by injection, although it does not appear to survive the acidic conditions of the stomach (Seena & Sridhar 2006).
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and enzyme inhibitors (trypsin and α-amylase inhibitors) that also affect the digestive process – although, again, their influence is substantially reduced by the cooking process. Toxic amino acids (canavanine, canaline) may be present, albeit in low amounts that are unlikely to result in poisoning. However, saponins that can cause nausea and vomiting are found in some species, particularly in inadequately processed seeds. Absorption of these compounds from the digestive tract is normally poor unless there is an injury to the gastrointestinal mucous membranes, as would occur in ulceration. The cyanide and tannin content, particularly after processing, tends to be quite low and unlikely to influence the seed’s nutritional value. A reduction in phytate content is similarly desirable as this component acts to bind minerals and decrease their absorption (Seena & Sridhar 2006; Ekanayake 2000).
Those who were wise in the ways of harvesting the tree carefully removed the latex-laden outer bark before cutting it down (Burkill 1935).
A Mangrove Poison
The Milky Mangrove (Excaecaria agallocha) exudes a characteristic milky, highly irritant latex, if the leaves or branches are damaged. Exposure can be particularly dangerous if the latex is accidentally splashed onto the sensitive eye membranes, which results in a temporary form of blindness. Indeed, this characteristic of the tree inspired the genus name, Excoecaria being derived from the Latin excaeco meaning to ‘make blind’. Over a century ago, the Government botanist Frederick Manson Bailey detailed the distress that could result from contact with the white sap: The most dangerous of the trees of this order [Euphorbiaceae] found in Queensland is Excaecaria agallocha, a small tree with somewhat fig-like leaves, often met with near salt rivers and swamps from Brisbane northwards. The trunk abounds in a most dangerous virulent acrid milk; woodcutters upon whom this juice has flown after a stroke of their axe, reported to Roxburgh that it produced inflammation and ulceration. [Georg Eberhard] Rumphius states that sailors who were sent ashore in Amboyna [Ambon Islands, Indonesia] to cut timber sometimes became furiously mad from the pain produced by the juice that fell on their eyes, and that some of them altogether lost their sight. The juice is a violent purgative (Bailey 1880).
Blind-your-eye or Milky Mangrove (Excoecaria agallocha), showing male flowers (against red leaves), female flowers (against yellow leaves) and fruit. The Milky Mangrove (Excoecaria agallocha) is a fairly widespread coastal tree,
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recorded that ‘workmen … had been often blinded, for four or five days together, by the white sap of a tree, which getting into their eyes, occasioned a most excruciating pain’. Joseph Maiden confirmed that the culprit was Excoecaria agallocha. In 1840 Dr James Stuart even observed the deliberate use of the plant to cause disability. Some convicts ‘produced permanent blindness by introducing into the eyes lime and the juice of the manchineal [sic] tree, a poisonous plant growing on the island’ (Gandevia 1981). The comparison of the toxic effects of native species to the Manchineel Tree is quite justified. The latter is native to Florida (USA), the Caribbean and Bahamas, Central America and northern South America.
A Poisonous Relative: The Dread Manchineel Tree
ranging from northern New South Wales to the northern tropics (Queensland, Northern Territory, Western Australia). There are a couple of subspecies which have sometimes been listed as separate species: the Milky Mangrove, E. agallocha var. agallocha (distribution: New South Wales to Northern Territory), and the Ovate-leafed Milky Mangrove, E. agallocha var. ovalis (distribution: Northern Territory to Western Australia) (Duke 2006). Milky Mangrove is found on landward mangrove sites around the high tide mark. It has made some interesting adaptations to its difficult environment, deploying a spreading root system to firmly anchor itself into its muddy habitat. The tree is very sensitive to water supplies and under conditions of scarcity tends to shed its leaves as a conservation strategy. During periods of severe drought it can lose them completely. The tree also produces both female and male flowers – the latter differentiated by a furry appearance and greater length.
Early experiences in Australia would appear to have been similarly intimidating. There are a number of records of children being made ill from mistaken identity or experimentation with the gum2 (Everist 1981; Hurst 1942). The Commandant of the first settlement at Norfolk Island, Philip King3, 2 Mention has been made of children in Queensland who mistakenly used the sap for chewing gum, thinking that it was the Moreton Bay Fig (Ficus macrophylla), and suffering fatal results. The references quoted are: Francis & Southcott 1967 and Cleland & Lee 1963 (see www.botanical-dermatologydatabase.info). I have, however, been unable to confirm these details. 3 King later became the third Governor of New South Wales.
Hippomane mancinella, from Phytographie Medicale by Joseph Roques, published in Paris in 1821.
The comparison of the Blind-your-eye Mangrove to the Manchineel Tree is based on more than a superficial resemblance. These trees have a relatively close relationship as both belong in the Euphorbiaceae family, in which latex-yielding species are characteristic. The latex of both species has similar acrid qualities. Indeed, cautions
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In 1871, the naturalist Dr TW Shepherd issued the following substantial warning with regard to the deleterious properties of Blind-your-eye Mangrove:
Hippomane mancinella (fruit). (Courtesy: Hans Hillewaert CC-BY-SA3.0 Wikipedia)
regarding the Manchineel Tree include instructions not to touch any part of it, nor to burn the wood. Even sitting underneath it during a rainstorm runs the risk of skin contact with the dissolved latex that can result in burns. The compounds responsible are tigliane phorbol esters that elicit symptoms almost identical to that of the Milky Mangrove: blistering, burns, erythema, swelling and inflammation. The fruits, which go by the intriguing title of ‘Death Apples’, live up to their name. They are highly toxic and contain physostigmine, which affects the nervous system via acetylcholinesterase inhibition. Accidentally mistaking them for an apple (which they closely resemble, hence the name Dwarf Apple Tree) can result in burning and swelling of the mouth, ulceration of the oesophagus, swelling and lymph gland enlargement. Extreme distress results, with an inability to swallow or talk, and progressive breathing problems can develop. Fatalities have occurred. Unsurprisingly, the latex was used as an arrow poison, to poison water supplies, and to deliberately inflict an excruciatingly painful death by tying the victim to the tree. The words of John Esquemeling, author of The Buccaneers of America (1678) provide a graphic illustration of the Manchineel’s virulent toxicity: ‘One day being hugely tormented with mosquitoes or gnats, and as yet unacquainted with the nature of this tree, I cut a branch thereof, to serve me instead of a fan, but all my face swelled the next day and filled with blisters, as if it were burnt, to such a degree that I was blind for three days.’
There is however, one plant about which little is yet known, but that little is interesting, and we think that it should not be passed by without notice. This tree Excoecaria agallocha was casually mentioned by Dr. Woolls F.L.S. of Parramatta in a lecture ‘On the Curiosities of Australian Botany’, recently delivered before the members of the New South Wales Horticultural Society. It is a native of the East Coast of Northern Queensland where it appears to be already known as the ‘Poison Tree’. This name appears to have been given to it without trial of its qualities, and indeed there is little danger of being wrong, in attributing a poisonous character to any newly discovered plant of this poisonous order. But in this case there has been something more than this to justify the name. We have been informed by a gentleman well known in Sydney, that on the occasion of a recent visit of his to Northern Queensland, he found specimens of this plant. In some of his rambles he was accompanied by one of the South Sea Islanders – so many of whom are now employed on the sugar plantations of the district. This islander, on seeing Excoecaria, at once recognised it as the tree from which, in his country, the natives procured the poison with which they render their arrows so deadly. Our friend expresses his conviction that the islander could not be mistaken, judging from his manner of expressing his recognition. Nor is it likely that he could be astray when it is considered of what great importance the tree must appear to his mind and the minds of all his countrymen. Probably it is looked upon by them with a superstitious awe, if not feared and venerated as of some Divine nature. We believe that it is generally understood that people who are wounded by these poisoned arrows seldom if ever recover from the effects. Since this recognition by the poor islander, people who are aware of the circumstances will be very cautious in dealing with this plant. And it is more than probable that … the information he has been the means of imparting may be the means of saving valuable lives. Not only this, but by attention, through him, being called to the plant, it is likely that its qualities will be enquired into long before it otherwise would have been. Without some casual circumstance this plant, like those we have mentioned in the earlier part of these notes, might have remained without examination for many years. Circumstances of this kind ought to lead to some recognition of the necessity for immediate steps being taken, with the view of organising some means for ascertaining the qualities
TALES OF MISADVENTURE of our natural vegetation. This is called for both to guard against qualities that may be deleterious to man as well as to his flocks and herds, and to take advantage of, or turn to use, qualities which it can
scarcely be doubted many of them contain. The whole world is interested in this. We are failing in one of our most evident duties to the whole human family, by so neglecting the matter.
A Well-known Toxic Genus
Mangrove habitat.
The Excoecaria genus contains around 40 species that range from tropical Africa and Asia to the western Pacific. Two are fairly widespread mangrove species, Excoecaria indica (which is not found in Australia) and E. agallocha. The latter has a wide distribution – ranging along the coastal regions of India and Sri Lanka to Japan, Southeast Asia, Malesia and tropical Australia (extending along the east coast into northern New South Wales). The poisonous latex, which is responsible for its name of Blind-your-eye Mangrove, is characteristic of a number of other species: E. macrophylla (Philippines), E. indica (Malaysia), and E. oppositifolia (upper Burma). Indeed, the latter has been responsible for serious cases of anaphylactic shock in lumberjacks. The caustic latex of E. grahami was also used for tattooing purposes in West Africa (Burkill 1935).
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Tribal markings resulted from the use of the freshly applied latex which caused swelling and black marks on the skin, the resultant scarification producing the desired skin designs. The African E. venenifera had a similar reputation. The milky latex, which was regarded as being highly toxic, could be ‘particularly injurious to the eyes’. Spirostachys africana is a closely related African species in the same family (Euphorbiaceae) that is hard to differentiate botanically, with equally injurious properties.4 Even the wood smoke was reputed to cause illness and headaches – although it was also said to have been utilised as a Sandalwood substitute (Verdcourt & Trump 1969). 4 Spirostachys africana, which has also been known as Excoecaria africana, contains diterpenes that are very similar to those found in Excoecaria parvifolia and E. agallocha (Grace 2007), as does the previously mentioned E. oppositifolia of upper Burma (Karalai 1994a).
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A Particularly Unpleasant Toxin
Unsurprisingly, the Milky Mangrove was employed as a deliberate poison in many places throughout its range from Asia to the Pacific Islands. In Australia Aboriginal people at Port Curtis (near Rockhampton, Queensland) used it as a poison for their spears, while in Papua New Guinea it was used as a piscicide and as an arrow poison (Hedley 1888; Everist 1981). It would appear that in some parts of Southeast Asia the tree was deployed with even more malicious intent. Henry Burkill mentioned that in Malaysia: [JD] Gimlette [in Malay Poisons and Charm Cures, 1915] … records the criminal use of the sap from the trunk, i.e. mostly latex, mixed with blood of a flying fox with the object of causing injury; it is calculated to produce strangury5 with haematuria and violent inflammation of the intestines. [In the 1890s the botanist M] Geshoff has recorded the criminal administration of the latex in the milk. Gimlette mentions it is put in toddy receptacles on palm-trees to stop theft: the toddy thief who drinks the sap intended for sugar-making is seized with violent pains after drinking it. The leaves are poisonous … Gimlette tells of the poisoning of waters by means of dried and powdered leaves. The latex quickly kills fish6 if dropped into water.
Burkill mentions its similar use as a piscicide in New Caledonia. In Malaysia, Milky Mangrove latex was employed as an adjunct to the sap of Antiaris toxicaria for making dart poison. However, Burkill makes a worrying comment on its medicinal use: ‘A little of the bark chewed, causes vomiting and purging, and may be resorted to in constipation by very strong people; but it is far too drastic for most people’. Similar use was made of the stem and bark sap. On Manus Island, in Papua New Guinea, the stem sap was deliberately taken to induce vomiting as an antidote for food poisoning (Holdsworth & Lacanienta 1981; Weiner 1985). One would have thought that these recommendations would only be resorted to by the incredibly desperate, or those unaware of the plant’s toxic reputation. Even so, there have been a few other medicinal 5 A highly discomforting urinary condition that is characterised by driplike micturition and extreme pain. It results in incomplete emptying of the bladder, which is persistently accompanied by feelings of great urgency. 6 Excoecaria cochinchinensis (syn E. bicolor) likewise contains a poisonous latex with piscicidal properties that was noted to kill fish more readily than E. agallocha (Burkill 1935). The piscicidal component of these plants has been identified as excoecariatoxin, which is composed of a daphnane diterpenoid ester and related compounds (Konishi 2003).
Antiaris toxicaria yields a lightweight timber and was utilised to make canoes and ornamental carvings by Aboriginal people in Australia. However, the sap within the bark has highly toxic properties and was particularly dangerous if eye contact occurred (Yunupinu 1995).
traditions that employed the tree. Australian Aboriginal people made a mashed bark infusion (heated) that could be rubbed over the body to ease pain and sickness (Roth 1903). Joseph Maiden mentioned that ‘the natives of Eastern Australia, as well as those of New Guinea etc., use this poisonous juice to cure certain ulcerous chronic diseases e.g. leprosy, but in Fiji the patient is fumigated with the smoke of the burning wood’7 (Maiden 1889). The latter could not have been a benign form of treatment. Maiden commented that the volatile character of the acrid milky juice was virtually inescapable: ‘no-one, however careful, can gather a quarter of a pint without being affected by it. The symptoms are an acrid, burning sensation 7 A similar procedure has been used for treating leprosy in Sri Lanka (Konishi 2003).
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in the throat, sore eyes, and headache’ (Maiden 1889). The fumigation process sounds quite appalling. It involved the preparation of a small fire of Milky Mangrove wood over which the leper was bound and suspended upside down, in the
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midst of the suffocating smoke, which was said to cause intense pain. The procedure was reputed to have cured some, although one would have expected a number of unfortunate participants did not survive the ordeal (Cambie 1986).
A Medicinal Milky Mangrove? Excoecaria dallachyana
Excoecaria dallachyana. (Courtesy: KAW Williams, Native Plants of Queensland, Vol. 4)
Excoecaria dallachyana. (Courtesy: KAW Williams, Native Plants of Queensland, Vol. 2)
Excoecaria dallachyana is an upland species found in the mountain ranges of southern Queensland and northern New South Wales (Duke 2006). The species name dallachyana commemorates the superintendent of the Melbourne Botanic Gardens, John Dallachy, who was associated with Ferdinand von Mueller in making early collections of botanical specimens from around the country (Baines 1980). In the Clarence River district of northern New South Wales, Excoecaria dallachyana was employed as a burn treatment. The site was smeared with snake fat and covered with a piece of bark, with some
of the juice (which shares the Milky Mangrove’s highly irritant properties) applied as a counterirritant. However, for severe pain the procedure became somewhat more dramatic. The juice was applied locally or glowing embers of the burning bark were used to cauterise the affected area. This strategy ‘was reserved for sufferers otherwise strong, two husky comrades holding the patient during this administration of the cautery’ (Cribb & Cribb 1981). Studies of bark extracts undertaken in 1956 showed a low level of antibacterial activity (Atkinson 1956).
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The Babesia Parasite
Babesia parasite. (Courtesy: CDC/Steven Glenn;
Lymphatic filariasis causing testicular enlargement. (Courtesy: l’ASNOM, asnom.org)
Selwyn Everist mentioned: ‘I have been told that it [Excoecaria agallocha] was used by some Australian Aborigines for the treatment of painful puncture wounds caused by sharp spines of some fish, especially Flathead (Platycephalus sp.). But no experimental confirmation of this has been noted in the literature’ (Everist 1981). In Fiji the plant was used for the removal of poisonous fish spines (such as those of the Stonefish) from the hand, which was held over a smoking fire made using fresh green leaves. Blood in the sputum was treated by chewing and swallowing the leaves, while a liquid pressed from bark was employed for fever and pain relief in those suffering filariasis (Weiner 1985). The latter is a very debilitating parasitic infection characterised by lymphatic oedema that can lead to elephantiasis (fluid retention leading to a massive, elephantlike leg) and hydrocoele (testicular enlargement). Interestingly, studies have shown that extracts of the leaf have anti-oxidant and anti-filarial activity with potential for use in clinical treatment protocols (Patra 2009).
Excoecaria cochinchinensis contains a compound called epiloliolide which is active against the tick-borne parasites Babesia canis and B. gibsonii that cause a haemolytic disease in dogs known as canine babesiosis (Yamada 2009). The infection, which is due to thread-like nematode worms, is prevalent throughout the tropics (Asia, Africa, Central and South America, Pacific Islands). The human form of babesiosis resembles malaria and is estimated to affect around 120 million people. Different species may be responsible: Babesia divergens in Europe and B. microti or B. duncani in the United States. The potential for more widespread infection could involve over a billion individuals. There is no vaccine and treatment options are limited, as well as often being ineffective. There can be serious side-effects with the potential for the development of drug resistance in the parasite and a high risk of reinfection (Patra 2009).
The use of Milky Mangrove sap or the leaf decoction as a remedy for ulcers has been recorded from Australia, New Guinea, India and Southeast Asia. One would expect that the caustic nature of the remedy would have involved some discomfort. However, a few other recommendations for the use of the leaves tend to suggest that, once processed, they do not retain the irritant attributes of the latex. In Fiji the decoction was
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even used to treat sore eyes, or chewed for an ‘unusual’ pain in the eyes, as well as to provide relief from a sore throat and headache (Cambie & Ash 1994). There is also mention made regarding the use of the sap from the young leaves and shoots, applied locally, to enhance enlargement and prolong penis stimulation in Papua New Guinea (Saulei & Aruga 1994). One could certainly have a few reservations about the latter recommendation. Henry Burkill mentioned that the roots appeared to be less poisonous than the aboveground parts of the plant. In Malaysia they were pounded with ginger to make an embrocation that was applied to swollen hands and feet. In addition an oily liquid that could be extracted from the boiled juice was used by the Burmese for skin disorders. The wood contains around 13–15% tannin. When subjected to destructive distillation it yielded a viscous oil that was similarly utilised (Burkill 1935). In Papua New Guinea, one drop of the sap was heated in coconut juice and taken to treat asthma or pneumonia. However, the remedy was used with great care as an overdose could easily occur and even a small dose had a purgative effect (Holdsworth & Lacanienta 1981).
The use of this mangrove as an abortifacient is probably not completely unexpected, considering the plant’s toxic reputation. The root was utilised in Papua New Guinea (Weiner 1985), and in Pakistan the latex was also used for the treatment of rheumatism, leprosy and paralysis (Erickson 1995). Henry Burkill mentions that Excoecaria cochinchinensis (syn. E. bicolor) leaf was applied externally for bleeding and for menstrual problems in Java, ‘apparently because they suppose an affinity between their red-bronze colour and blood’. This recommendation may have more to it than mere coincidence. Thai herbal physicians have employed both Excoecaria agallocha8 and E. bicolor as a female tonic. Interestingly, leaf extracts of the latter species contain diterpenes with uterotonic properties (Karalai 1995). In Vietnam this species was utilised similarly – as well as for the treatment of skin disorders (furuncles or infections of the hair follicle, and pruritus), diarrhoea and dysentery. Studies have shown that leaf extracts contain flavonoids (including kaempferol and derivatives), phenolics (gallic acid), shikimic acid and glycosides (excoecariosides) (Giang 2005). 8 Thai medicine also makes use of the bark and wood of Excoecaria agallocha as a remedy for flatulence (Konishi 2003).
Bioactive Diterpenes
Blind-your-eye Mangrove has distinctive knotty roots that spread over a wide distance. The roots, which are not vertical blind branches as in other shore trees, are thickened horizontal segments richly furnished with lenticels. They protrude above the mud into which the feeding roots branch (Burkill 1935). (Image courtesy: KAW Williams, Native Plants of Queensland, Vol. 3)
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The herb Daphne genkwa, which has been employed as an abortifacient in traditional Chinese medicine, contains similar chemical components to those found in Excoecaria. They include skin irritants of the daphnane (e.g. yuanhuacine) and tigliane type that are found in the latex of Excoecaria acerifolia, E. agallocha, E. bicolor and E. parvifolia (Grace 2007; Karalai 1994a, 1994b; 1995). Unfortunately diterpene esters have tumour-promotion effects that have led to reservations regarding their carcinogenic and irritant potential (Konishi 2003; Karalai 1995). However, other constituents also appear to be present with anti-carcinogenic activity; e.g. Excoecaria agallocha (wood and leaf extracts) contain diterpenoids with anti-tumour promotion properties (Konishi 1998). Indeed, compounds with anticancer potential (antiangiogenic and apoptosis-inducing activity)
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expansum (Vadlapudi 2009). Studies of bark extracts (ethanol) indicated equally interesting pharmacological potential. This included antibacterial activity against Shigella, Enterococcus and Staphylococcus aureus. Bark extracts, which exhibited a low level of toxicity, were found to possess marked sedative and central nervous system depressant activity (Subhan 2008a). There are also reports of gastroprotective effects comparable to cimetidine which could be useful for the treatment of stomach or duodenal ulceration – as well as potent analgesic properties comparable to the NSAID drug diclofenac sodium (Subhan 2008b).
An Australian Gutta Percha
Daphne genkwa. (Plate from Flora Japonica, Sectio Prima (Tafelband), Philipp Franz von Siebold and Joseph Gerhard Zuccarini 1870)
from Excoecaria acerifolia have shown interesting activity against lung cancer cells (Zhao 2010). In addition, diterpenes from the genus have attracted interest for their anti-fouling potential against the marine animals (barnacles, mussels, tubeworms and seaweeds) and micro-organisms (Pseudomonas pseudoalcaligenes) that colonise the underside of boats (Wang 2009).
Surprisingly, drug research has taken a serious interest in the Milky Mangrove. Investigations have supported its potential as an antiviral, anti-HIV, antibacterial and anticancer agent (Peter & Sivasthothi 1999). Extracts (leaf, stem) have shown anti-HIV activity, with leaf extracts possessing substantial antioxidant effect that was attributed to ellagic acid (Subhan 2008c; Zou 2006; Konoshima 2001; Masuda 1999; Erickson 1995). Studies of the antimicrobial properties of leaf extracts established that chloroform and methanol (but not hexane) extracts were the most effective. In particular, methanol extracts had a good spectrum of antifungal activity and were particularly active against Acremonium strictum and Penicillium
Excoecaria parvifolia. (Courtesy: Ranganathan, CMKb9)
Prof.
Shoba
The Gutta Percha of the Gulf of Carpentaria (Excoecaria parvifolia) had a very similar 9 Gaikwad J, Khanna V, Vemulpad S, Jamie J, Kohen J,Ranganathan S. 2008. CMKb: a web-based prototype for integrating Australian Aboriginal customary medicinal plant knowledge. BMC Bioinformatics. 9 Suppl 12: S25.
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reputation to the Milky Mangrove, although its medicinal use differed somewhat. Dr Thomas Lane Bancroft mentioned injuries associated with timber cutting activities when some of the juice splashed onto the hands or eyes: ‘they then become for a time blind. This blindness is only of short duration, leading to no after effects’ (in Maiden 1900b). Edward Palmer commented on its medicinal reputation: ‘The natives use the bark mashed up in water in a wooden kooliman, and heated with stones from a fire close by. The wash is applied externally to all parts of the body, rubbing it in. Used for pains and sickness’ (Palmer 1883). This remedy continues to be utilised today. The bark or leaves are decocted (boiled) to make a cloudy red liquid that is applied locally as a healing antiseptic wash for cuts, sores, boils, scabies, rashes, chicken pox sores, and various other skin conditions. The liquid has been rubbed over the body (joints, back or chest) and as a first aid application on injuries to reduce swelling and provide pain relief. Its use, however, is not recommended for the face and great care is taken to avoid getting the liquid in the eyes. It also
had a tonic reputation and bathing in the infusion was said to make weak and tired individuals feel stronger (Wightman 1994; Barr 1988, 1993; Smith 1993). A large number of diterpenoid components have been isolated from Excoecaria parvifolia, as well as the triterpene lupeol (Grace 2007). The fragrant timber of Excoecaria parvifolia has been utilised for making tools, long-stemmed smoking pipes, weapons (nulla-nullas) and boomerangs. The wood can be burnt as an aromatic repellent for mosquitoes – although only the dry timber is used for the latter, thereby avoiding any contact with the latex. The leaves, bark or twigs are also suitable for use as a poison to stun fish, which are cooked before being eaten (Lindsay 2001; Wightman 1992 & 1994). Damaged Milky Mangrove (Excoecaria agallocha) growing in challenging coastal environments yields a similar aromatic timber known as Bastard Aloeswood, procured from trees that had been severely weathered by sun and sea exposure. The resinous, highly fragrant timber was, however, so rare as to be impossible to find in commercial trade (Burkill 1935).
The Fearful Finger Cherry Rare Rhodomyrtus The genus Rhodomyrtus contains around 15 species that are found ranging from Australia to Asia, Malaysia and Melanesia. There are seven Australian species, four of which are endemic to the rainforest of tropical Queensland: Rhodomyrtus canescens, R. effusa, R. pervagata and R. sericea. Two species have a wider distribution, extending to central Queensland – the Ironwood Rhodomyrtus trineura (which has two subspecies: capensis and trineura) and the poisonous Finger
Cherry (R. macrocarpa). R. psidioides is found in southern Queensland (Sunshine Coast) ranging to northern New South Wales. Rhodomyrtus tomentosa refers to an AsianMalesian species known as the Mouse Guava, which was erroneously recorded from Australia in earlier literature. A couple of other species have been re-classified: Rhodomyrtus beckleri is now Archirhodomyrtus beckleri, while Rhodomyrtus recurva refers to Pilidostigma papuanum.
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Leaf and flower of the Rusty Rhodomyrtus (Rhodomyrtus pervagata).
Leaf and flower of the rare Grey Rhodomyrtus (Rhodomyrtus effusa). (Right) The Ironwood Rhodomyrtus trineura (originally classified as Myrtus trineura), was formerly classified in three varieties: var. canescens (now R. canescens), var. macrophylla (now R. pervagata) and var. trineura (R. trineura).
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There are some unexpected floral hazards in the tropical Australian forest. One of the most deceptive would be a rather tasty-looking fruit known as the Finger Cherry (Rhodomyrtus macrocarpa). This small shrubby tree is found on the outskirts of lowland rainforest and belongs to the same family as the Eucalypt (Myrtaceae). It grows on poor soils in high rainfall areas of the Australian and Papua New Guinea tropics. In the early 1900s consumption of the Finger Cherry was found to have some rather serious, and seemingly unpredictable, consequences. The mature fruit, which was harvested by Aboriginal people, was very sweet, although it was not usually eaten in large amounts. The fruit was rubbed in the sand to peel away the skin and then eaten raw – although it tended to induce a feeling of dryness in the mouth. If the harvest was large enough the Finger Cherries were taken back to the camp to be baked in hot ashes. Between 1892 and 1915 disturbing reports began to circulate regarding incidents of blindness that had resulted from eating Finger Cherry fruit. On 20 September 1894, the following appeared in the Sydney Morning Herald: ‘Cases of sudden loss of sight have been reported on several occasions from Cairns. It was generally believed that this was brought about after persons had eaten of a peculiar berry, known as ‘finger’ or ‘native loquat’, which grows plentifully in the district. A sample of the berries was received by the Colonial Botanist. He found them to be badly infested with fungus, but there was no trace of poison’ (Maiden 1900a).
Developing fruit from Rhodomyrtus macrocarpa. The green fruit matures to turn a bright red colour that takes on a darker hue when ripe. As they mature the fruit elongate, acquiring a jointed finger-like appearance due to the growth of the seeds embedded within the fruit flesh.
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The fungus was identified as Gloeosporium periculosum, which FM Bailey, in 1895, had graphically described as ‘pustules occupying the whole or part of the surface of the ripe fruit, forming sulphur-coloured nodules beneath the cuticle’. The tree quickly achieved notoriety, as its drastic effects became the subject of rumour and innuendo. No one truly knew why the fruit had such terrible consequences and many who had partaken of it in the past were extremely worried. In 1910 Edmund James (Ted) Banfield wrote eloquently of the situation in his Confessions of a Beachcomber – a classic tale that recorded details of life on Dunk Island: The finger cherry ‘Pool-boo-nong’ of the blacks (Rhodomyrtus macrocarpa) possesses the flavour of the cherry guava, but has a most evil reputation. Some assert that this fruit is the subject of a certain disease (a kind of vegetable smallpox), and if eaten when so affected is liable to induce paralysis of the optic nerves and cause blindness and even death. Blacks, however, partake of the fruit unrestrictedly and declare it good on the authority of tradition as well as by present appreciation. They do not pay the slightest respect to the injurious repute current among some white folks … At any rate blacks are not affected by the fruit, although large consumers of it, and many whites also eat of it, raw and preserved, without fear and without untoward effects.
Unfortunately, Banfield’s assumption was untrue. Serious incidents of blindness were reported by Aboriginal people. In 1944 a comprehensive review of the situation by Dr Hugo Flecker appeared in the Medical Journal of Australia. He commented: The story reads rather like a fairy tale fit only for children: but actual investigation shows that it is not far from the truth, as further victims testify. Today, every adult in North Queensland is fully aware of the existence of the plant and of its evil reputation, and whereas in former years it was commonly eaten by all inhabitants, white and aboriginal alike, it is now never mentioned or seen without being pointed out as a fruit especially to be avoided. Probably this propaganda in school has prevented many further cases of blindness. The evil reputation of this plant has reached abroad, for in June 1936, Dr. J. Ringland Anderson received inquiries from Russia ‘concerning its toxic effect on the eyes’, while more recently a request has come from Cuba for specimens for experimental purposes.
The loss of vision could be extremely abrupt. One victim described its onset as being ‘like a streak of lightning.’ In 1892 one of the earliest incidents of Finger Cherry-induced blindness involved a four-yearold girl, whose father ‘had eaten the fruit for many years, but her mother disapproved of this. After eating the fruit, somewhere about midday, the patient went to bed as usual, feeling very well; she could see well … Next morning at about 6 o’clock while the sun was shining brightly outside, she was playing with her father and could see well. Ten minutes later, however, while in her mother’s company, she was unable to see anything at all’ (Flecker 1944). Other reports gave similar details of incidents characterised by an abrupt onset of blindness, with varying degrees of recovery. None of the cases recovered full eyesight and the majority lost it completely, at least in one eye. The blindness was the result of ‘optic atrophy’ – degenerative changes of the optic nerve. In the late 1800s and early 1900s the situation in the Cairns area bordered on general panic. The cases of blindness usually occurred in young children, which was of grave concern to the community. In 1915 a graphic education program was initiated to warn school children of the danger: ‘Public opinion must have been considerably stirred by the succession of victims and the Department of Education … caused full-sized coloured posters of the plant showing flowers, leaves, fruit et cetera to be hung in all schools throughout North Queensland’. The text of the posters reflected the strong emotion that surrounded the subject: ‘Think of it, children! Never to see the sunlight again, the trees, the flowers, the faces of your companions and your loved ones. You would sit hour after hour in your home, unable to read or to write, unable to romp and play games, always, always about you the dark blackness of eternal night’ (Flecker 1944). Although rare, incidents of blindness from eating the fruit had also occurred in animals, mainly goats and calves. Fortunately, the plant was not normally found growing around grazing sites. The exact cause of the problem was the subject of great debate. While it was widely proposed that infestation with the fungus was the culprit, there was also the proposition that an unidentified chemical compound in the fruit could be responsible. Extermination of the tree appeared to be the only
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Flowering Finger Cherry shrub (Rhodomyrtus macrocarpa).
practical answer: ‘Whenever you know of a Finger cherry tree growing, tell your parents and ask them to have it destroyed, Never eat or handle or have anything to do with Finger Cherries, lest you become like one of the children of whom we have just read’ (Flecker 1944). In a review of Australian Plants and Chemical Research (1969), Professor Len Webb, who had a somewhat broader viewpoint, commented: ‘Small wonder that nervous fathers proceeded to hack down every Finger Cherry tree in sight in the Cairns district! This rather primitive reaction, in the absence of any attempt at scientific investigation of the plant’s properties, reminds one of the natives of Calabar in Nigeria. They used to destroy the poisonous Calabar Bean (Physostigma venenosum) wherever they found it. Later the plant was shown to contain the drug physostigmine, used in ophthalmology, and became a valuable article of export.’
Confusing Case Histories
Despite the reports, however, not all were convinced of the fruit’s toxicity. In 1943 Dr E.O. Marks wrote:
I asked Dr. J. Lockhart Gibson, as being the oldest eye specialist here, and for so many years ophthalmologist to the Children’s Hospital … He told me he had never seen a case which he could definitely prove to be due to eating finger cherry. I have seen one case of optic atrophy, not of recent origin, which was attributed to the finger cherry, but as far as I remember now the evidence was not convincing, let alone conclusive. My impression from Dr. Gibson was that he is very sceptic[al] as to the finger cherry causing optic atrophy (Flecker 1944).
Dr Gibson’s attitude was not very surprising considering that the details of most reports were quite sketchy. It was difficult to find accurate information on the topic for research purposes. A little later, in 1945, 27 soldiers in Papua New Guinea suffered blindness due to eating the fruit. However, the report of this disturbing incident lacked any details that would shed light on the situation. Many accounts contributed contradictory elements. In a case recorded in 1947 one child, who had eaten green fruit and had rubbed his eyes, lost his sight – while four other children in the same group ate mature fruit and remained unaffected (Everist 1981). Selwyn Everist summarised the evidence:
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Fruiting Finger Cherry Tree. There is no agreement concerning the stage of maturity at which the fruits are toxic, but there appear to be three different schools of thought. One opinion is that the fruits are toxic in the immature stages, either green or a clear bright red. A second opinion is that only the overripe fruits are poisonous and a third opinion … is that the fruits are probably toxic only when infested with the fungus Gloeosporium periculosum. The only common factor noted in all the published case histories is that all the victims ate large amounts of fruit in a short time.
The report by Dr Flecker in 1944 is illustrative of the problem. He provided details regarding five cases: two had consumed over-ripe fruits, a further two had eaten immature fruit, and the information regarding one case was incomplete. The accuracy of the information had been marred by the passage of time because all the cases were reviewed a long time after the incident. Indeed, lapses of between 15 and 52 years were involved. However, one fact was certain – the effects could be dramatic. The loss of sight appeared to occur at random and with utter unpredictability. The blindness was often total and irreversible. The case histories given in Dr Flecker’s paper, although interesting, make tragic reading:
A female aboriginal and an intelligent inmate of Yarrabah Mission Station, at the age of eight years (towards the end of 1929) ate a great many ‘cherries’ direct from the tree. The older girls had eaten the ripest, leaving only the halfripe and immature fruit. This was the first occasion on which the patient had tasted them. The older children were not affected in any way. For two weeks afterwards she was able to see well: but then a ‘boil’ appeared on the inner canthus of her right eye. One Saturday she was not able to see well, but the next day everything appeared black, and she could see nothing at all. For a whole year she had to be led around: but her condition slowly improved, vision being slightly better in the right eye than in the left eye. She is now able to see her way round and can count fingers, although she was unable to recognise an object such as a shoe.
Another report from Yarrabah mentioned that a different girl: [had eaten] some finger cherries near the Mission Beach, picking them from the bushes; but she does not remember whether any were gathered from the ground. She had eaten them every day, but always on the same day they were picked, the fruit was ripe, but not over-ripe. She says that her blindness took place the day before that of the preceding patient, although she did not accompany
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the other girl (this is denied by the other … who states that S10 accompanied her, and that both had to eat unripe fruit as other children had picked all the mature cherries). Although S’s eyesight had previously been good, one morning she was unable to see anything, and she cried a great deal. Her right eye had apparently recovered in three days, but she was unable to see with the left. She was able to attend school.
A particularly puzzling aspect of the situation was the fact that numerous people had regularly eaten the fruit for many years without encountering any serious problems. It was claimed that the ripe fruits could be eaten with impunity: ‘The late Fred Martin of El Arish knew this, and ate a full plate of selected ripe Finger Cherries without ill effects, before a visiting team of scientists a few years ago’ (Webb 1969). It is possible that there are chemotypes of the plant that were more toxic than others, or that the toxic component was only present during certain stages of the ripening process. In 1954 the University of Cambridge investigated samples of Finger Cherries, both ripe and immature. These studies revealed that the immature fruits contained a toxic substance (a dibenzofuran) that was named rhodomyrtoxin. Although it was toxic to mice, studies on a possible selective action on the optic nerve were not undertaken due to technical difficulties (Webb 1969). It is an intriguing tale which has remained unresolved. There is only one other study of the mature fruit, done by Nancy Atkinson in 1956, who undertook an evaluation of antibacterial substances from flowering plants. She determined that extracts had antibacterial properties against Streptococcus typhi, Mycobacterium phlei and Staphylococcus aureus. Interestingly, initial studies of a related species, the Mouse Guava (Rhodomyrtus tomentosa), showed antibacterial properties against Staphylococcus aureus and Escherichia coli. Additional studies have confirmed a good spectrum of antibacterial activity against Bacillus (B. cerecus, B. subtilis), Enterococcus faecalis, Staphylococcus (S. aureus, MRSA, S. epidermidis), and Streptococcus (S. gordonii, S. mutans, S. pneumoniae, S. pyogens, S. salivarius). These findings led to the isolation of an active antibacterial compound called rhodomyrtone, with strong bactericidal activity and 10 Name withheld in original text.
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good potential for clinical development. In particular, it has been suggested for use against staphylococcal skin infections and Streptococcus pyogens (Limsuwan 2011, 2009; Sianglum 2011, 2010; Limsuwan & Voravuthikunchai 2008; Saising 2008; Dachriyanus 2002). This has also resulted in a suggestion for the use of Mouse Guava extract as an antibacterial preservative for food products (Voravuthikunchai 2010).
Essential Oils from Native Rhodomyrtus
The essential oils of the native Rhodomyrtus species tend to be pinene based, which suggests they may have good antimicrobial and anti-inflammatory properties. The aromatic components aromadendrene, limonene, spathulenol and viridiflorol are present in some species. Globulol also has antibacterial and fragrance attributes. Limonene is of particular interest because it has antimicrobial, antiviral and anti-inflammatory properties, as well as anticancer and anti-allergic potential. Caryophyllene is likewise antiseptic and antiinflammatory, with anticancer and anti-parasitic
Rhodomyrtus canescens.
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Rhodomyrtus psiodioides.
potential. Species with pinene-rich oils (monoterpene and sesquiterpene based oils): • R. canescens: α-pinene (20–23%), β-pinene (6– 10%), aromadendrene (12–17%) • R. pervagata: α-pinene (27–35%), β-pinene (18–24%) • R. psidioides: α-pinene (28–66%), limonene (1–24%) • R. sericea: α-pinene (28%), β-pinene (21%), β-caryophyllene (13%). Species with complex oils (low monoterpene levels): • R. trineura subsp. capensis: α-pinene (trace–26%), globulol (9–19%), viridiflorol (5–12%), spathulenol (4–7%) • R. trineura subsp. trineura: β-caryophyllene (16– 29%), caryophyllene oxide (2–12%), globulol (7–10%) • R. effusa: globulol (11–22%), viridiflorol (8– 10%), spathulenol (5–18%) • R. macrocarpa: β-caryophyllene (9–44%), aromadendrene (6–11%) globulol (8–10%).
Rhodomyrtus sericea.
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The Medicinal Mouse Guava The Mouse Guava (Rhodomyrtus tomentosa) is an interesting relative of the Finger Cherry with a diverse medicinal career. The leaves, which have a leathery character with a distinctly hairy underside, were employed for treating wounds in Indonesia. In Vietnamese and Malaysian traditional medicine the leaf was regarded as having equivalent astringent qualities as those of Guava (Psidium guajava) – a related herb with a good reputation as an antidiarrhoeal agent (Perry & Metzger 1980; Burkill 1935). In Vietnam, powdered leaves of the Mouse Guava (combined with an extract of Caesalpinia sappan) was also regarded as being highly effective for diarrhoeal disorders. This is supported by studies showing that extracts had antimicrobial properties against Staphylococcus aureus, Diplococcus pneumoniae, Bacillus mycoides and Streptococcus haemolyticus (Duc Minh 1993). Chinese medicine has utilised the Mouse Guava similarly for gastrointestinal distress. It was recommended as an antidiarrhoeal and tranquillising agent valued for acute gastroenteritis, chronic dysentery, hepatitis and low back pain. In addition, the dried fruits were employed as a tonic for anaemia during pregnancy, debility following illness, and for treating neurasthenia (Hong Kong CMRI Vol. 1 1984). In Malaysia the roots provided an ingredient in tonic mixtures that were usually taken by mothers after childbirth (Zakaria & Mohd 1994). Indonesian healers utilised the root decoction as a tonic, while in Brunei the leaf juice, as well as the fruits, were regarded as being useful for anaemia. Interestingly, the fruit has even been eaten to encourage wound healing (Haji Modhiddin 1992). In addition, there is an intriguing reference to a Malaysian remedy that mentions the use of the root infusion for treating scars on the cornea of the eye, with the concurrent application of a leaf poultice to the head (Burkill 1935). The Mouse Guava (Rhodomyrtus tomentosa) is a small tree native to China, India and Southeast Asia, the Philippines and some Indonesian islands (Sulawesi). The colourful pink flowers yield attractive purple-black fruits.
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Blue Lily Toxins
it being reported as a poison plant here. But in Western Australia, it is much more abundant than it is with us, and it has so frequently and so consistently been reported as the cause of ‘Blind Disease’, that there appears to be no room to doubt its poisonous nature (originally cited in JH Maiden 1894).
In 1920 the Chief Inspector of Stock of Western Australia provided the following information with regard to feeding experiments: portions of the plant being fed to rats with the result that blindness occurred on the second day, the whole ration being three grains. In many cases sheep have been badly affected with blindness as a result of eating this plant. Horses … have not infrequently suffered from partial paralysis of the hind quarters when depasturing on country where the plant is fairly prevalent. Its effects seem to vary in different districts, but so far all tests up to the present have given positive results. The plant appears to be most injurious in the early winter and before other plants have become fully established (Henry & Hindmarsh 1923).
Nodding Blue Lily (Stypandra glauca). (Courtesy: Cygnis insignis, Wikimedia Commons Project)
The Nodding Blue Lily (Stypandra glauca), although apparently not hazardous to humans, is another native plant that can cause blindness in animals. This attractive lily-like plant, which is placed in the Hemerocallidaceae (formerly Liliaceae), resembles the blue-flowering Flax Lilies (Dianella spp.), to which it is closely related. Nodding Blue Lily is native to southern Australia (Western Australia, South Australia, Victoria and New South Wales), extending to southern Queensland. It is also found in New Caledonia. The plant has long been known as a stock poison that can cause blindness. A report by the government veterinary surgeons Max Henry and WL Hindmarsh in 1923 provided the following details, attributed to a Mr Ash, who stated: This is a herb which is stated to cause animals that have been fed on it to go apparently blind and run into any sort of object. It seems to be the least fatal of all the poison plants. It is slower in taking effect. This plant is common in the neighbourhood of Sydney, the Blue Mountains, and many other parts of the Colony, but I have never heard of
Nodding Blue Lily was also associated with the death of sheep and symptoms of nervous irritability in cattle (Henry & Hindmarsh 1923). Selwyn Everist (1981) detailed research (under Stypandra imbricata) that confirmed the young shoots could cause central nervous system degeneration and retinal atrophy – no wonder it acquired the name ‘Blind Grass’. Later studies identified various neurotoxins, including styphandrol and styphandrone, which were also present in the Blue Flax Lily (Dianella revoluta). However, the toxicity of the fresh plant was not the same as that exhibited by the isolated compound (Colgate 1987 & 1986). In addition, its potential blinding effects could vary according to season. A study of goats determined that this occurred only when the plant was flowering (Whittington 1988). The genus Dianella contains 20–30 species with a fairly wide distribution, ranging from Japan to India, to Australia and New Zealand, with a few species being found in the Pacific Islands. Aboriginal people widely utilised Flax Lilies for weaving purposes. These plants have a variable reputation as a bush food, with some species being considered palatable and some not. The roots of Dianella laevis (now D. longifolia) and D. caerulea were pounded and roasted on hot
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Hemerocallis fulva, Daylily, by Prof. Dr Otto Wilhelm Thomé, Flora von Deutschland, Österreich und der Schweiz 1885, Gera, Germany. Styphandrol has also been found in Daylilies (Hemerocallis spp.), which belong to the same family as the Flax Lilies and Blind-grass. A compound isolated from the Daylilies was originally given the name hemerocallin, but this was later found to be identical to the neurotoxin in Styphandra glauca (Wang 1989).
rocks (Leiper 1984). Studies have shown that baked Flax Lily roots (D. laevis) had a low glycaemic index (Thorburn 1987). The fruit of a few Dianella species have also been considered edible, albeit rather insipid in character – with some species being more palatable than others. However, despite their luscious appearance, it would appear wise not to try too many. Dianella caerulea flowers and fruit.
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On June 7, 1942, when on a survey of edible native plants at Yarrabah [near Cairns] … Mr JH Buzacott … had the following interesting experience after tasting a fruit of this plant … Mr. Buzacott writes … ‘I therefore decided to crush one of the fruits and taste it. The crushed berry was simply dabbed on may tongue and very little flavour was noticeable. I did not swallow, but expectorated freely in case there was a poison present in the juice. We then proceeded along the tract at a steady marching pace. Within a few minutes after tasting the fruit, I had a feeling that I was going to the left all the time, and I felt that I had to force myself to march to the right in order to keep in a straight line … the feeling was accompanied by a slight dizziness. It was only a matter of minutes before I was unable to walk straight at all, and in spite of all attempts, I could only walk to the left hand. I therefore sat down in the shade. The only feelings I can recall are a slight churned-up feeling internally and slight dizziness. Within 10 minutes I was able to resume the march, apparently quite recovered.
Dianella tasmanica. The fruit of this species are unpalatable, having a bitter and astringent character, and may well be poisonous.
Despite the link with these neurotoxins, the toxicology relating to the Flax Lilies (genus Dianella) remains somewhat obscure. Some have been suspected stock poisons, although this remains unconfirmed (Everist 1981; Webb 1948). Reports of incidents of poisoning are quite rare, and fairly old. For instance, Evelyn Hurst (1942) noted that ‘the fruits of D. intermedia are considered poisonous in New Zealand.11 In 1891 there is a record of a child of twenty-one months being poisoned by them. The symptoms were laboured respiration and hiccough. Death occurred about 18 hours after the fruits were eaten. D. nemorosa is an exotic species which is regarded as poisonous in the tropics.’ Dianella ensifolia roots have been regarded as poisonous in Chinese and Southeast Asian herbal traditions (Duke & Ayensu 1986). Len Webb (1948) provided another intriguing report with regard to Dianella caerulea in northern Queensland: 11 Dianella intermedia is also found in New South Wales.
The plant identity was verified and the account fully substantiated. The Aboriginal guides said that the plant was not used by them, although fruit was reputedly eaten by goannas after fighting with a snake ‘to kill the venom’ (Webb 1948).
Dianella Dye
Flax Lily fruit.
Dianella berries are distinguished by an eyecatching vivid blue, suggestive of a rich dye substance that inspired the explorer Christie
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Palmerston to experiment with their use: ‘Plucked some berries which make splendid ink. They grow on a pretty bush bearing a blue flower. Outside they are green [immature fruit], but inside is of a deep bluish black. I just bruised them, boiled them in a little water, strained the product through a pocket handkerchief, and the result was a capital blue ink fluid’ (Savage 1989). George Bennett mentioned a similar use of a native Hawaiian species: ‘a species of Dianella … bearing a quantity of mazarine-blue berries, which are used by them as a permanent blue dye’. The brilliant blue pigmentation of Dianella fruit is due to anthocyanin compounds, notably delphinidins and a naphthalene glycoside (Bloor 2001). This species has the typical clumping lily-like character of the genus. The brilliant blue-coloured fruit yield a useful dye for colouring kapa (tapa) cloth. Dianella sandwicensis is of interest as a unique endemic that is the sole representative of the Hemerocallidaceae family in the Hawaiian Islands. Some classifications now place this as a sub-family of the Xanthorrhoeaceae, to which the famous Australian Grass-trees (Xanthorrhoea spp.) belong.
Dianella sandwicensis fruit and flower. (Courtesy: Kim and Forest Starr, Hawaii)
Not a lot is known about the medicinal uses of Australian Dianella species, although older reports mention the use of the roots as a treatment for dysentery, as well as for genitourinary disorders (dysuria, leucorrhoea, blennorrhoea). In Malaysia it
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has been utilised as a fragrance and medicinal herb, as Henry Burkill (1935) reported: The hard roots descending from the rhizome possess a characteristic smell and it is these that are most used. The smell is not aromatic. If they are chewed, after being dried, they are sweetish ... They enter into cosmetics and into poultices applied to the abdomen as vermifuges. They are used for fumigations and the ashes of root and leaves are part of an ointment for herpes. [The] leaves used for poulticing wounds … [and] given to stimulate [the] appetite of elephants. It was said that the roots could be used as a rat poison, but this use is not proved.
The application of the leaf poultice for wounds, abscesses and various abdominal problems appears to be quite well known. The root decoction has also been taken following childbirth as a strengthening remedy in the Philippines, while in Indonesia the leaves were poulticed on the back to treat lumbago (Hirschhorn 1983; Perry & Metzger 1981). In addition, the root decoction of Dianella ensifolia was regarded as a useful treatment for hepatitis and jaundice in Brunei, with a small amount being drunk (bin Haji Mohiddin 1991). Australian investigations have shown interesting pharmacological properties for a few native species: Dianella callicarpa root demonstrated significant antimicrobial and antiviral activity, which was due to a naphthalene glycoside (dianellidin) (Dias 2009). This compound is a precursor for styphandrone, which has raised concerns about the toxicity of the herb. Dianella longifolia var. grandis root extracts were antiviral against poliovirus. Chrysophanic acid, an anthraquinone, was identified as the anti-poliovirus component. The roots of Dianella revoluta var. revoluta, which has been utilised as an Aboriginal remedy for colds and general sickness, also had weak antiviral activity against human cytomegalovirus (Semple 2001, 1998). Recent studies have shown that Dianella ensifolia extracts had potent antioxidant and tyrosinase-inhibitory activity with potential for use as a skin-whitening cosmetic. Its activity compares very favourably with hydroquinone, a commercial product used for this purpose (Mammone 2010; Nesterov 2008).
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Stinging Tree Infamy Native Stinging Trees
Dendrocnide photinophylla.
Stinging Tree (Dendrocnide cordifolia).
Large ‘nettle-like’ shrubs with highly irritant stinging hairs over the leaves are characteristic of the Dendrocnide genus, of which around 37 species are known. Their botanical classification formerly placed them in the genus Laportea, by which name they were widely referred to in much of the older literature. There are eight Australian species that can usually be distinguished by differences in their distribution. Those restricted to northern Queensland include Dendrocnide cordata, D. cordifolia, and D. corallodesme. The latter, which is fairly rare, is only known from the Iron and McIlwraith Ranges on Cape York, although it is found in Papua New Guinea. The Gympie Bush (Dendrocnide moroides), which is also found in Malesia, has a wider distribution along the Queensland coast to the New South Wales border. The Mulberry- or
Shining-leaved Stinging Tree (D. photinophylla), which has a similar distribution, is also found in northern New South Wales. The Giant Stinging Tree (Dendrocnide excelsa, formerly Laportea gigas) ranges further south, from southern Queensland to the Victorian border. In addition, there are a couple of offshore species: D. peltata is found on Christmas Island, with two varieties (var. peltata and var. murrayana) ranging to the Cocos (Keeling) Islands, where D. sinuata is also found. D. peltata var. peltata is also found in Java, Bali and New Guinea. One of the greatest hazards of the Australian rainforest is the infamous Stinging Tree (Dendrocnide spp.). This is a pioneer genus that has been an important, and often underestimated, obstacle that all the early explorers tangled with in the rainforest. The tree readily colonises disturbed areas, favouring sunlit areas along walking tracks and rivers. The large heart-shaped leaves acquire a dull green appearance due to their covering of fine hairs which are renowned for causing various degrees of pain (depending on the species) on even the slightest contact. Once stung the pain, which can be quite agonising, periodically recurs with the slightest stimulation of the area. The discomfort can last for months and is an experience not easily
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forgotten. While exposure to the Stinging Tree does not appear to have been associated with fatalities, some quite dreadful injuries have been reported. Records of incidents involving soldiers in the Queensland jungle mention that the victims became ‘quite frantic, dashing about violently and rolling on the ground’ (Webb 1948). In 1889 Carl Lumholtz wrote graphically of his encounters with the infamous plant:
A Hazardous Bushfruit Harvest
One of the greatest annoyances in this almost inaccessible region is the poisonous nettle, the stinging-tree (Laportea moroides). It is so poisonous that if its beautiful heartshaped leaves are only put in motion they cause you to sneeze. The fruit resembles raspberries in appearance, the leaves are covered with nettles on both sides, and a sting from them gives great pain. It will make a dog howl with all his might; but it has an especially violent effect on horses. They roll themselves as if mad from pain, and if they do not at once receive attention they will in this way kill themselves, as frequently happens in Northern Queensland. The natives greatly dread being stung by this nettle, and always avoid it. If you are stung in the hand you soon feel a pricking pain up the whole arm, and finally in the lymphatic glands of the armpit. You sleep restlessly the first night. The pain gradually leaves the arm, but for two to three weeks you have a sense of having burned your hand if the latter comes in contact with water, for then the pain at once returns where you were stung by the nettle.
Other early explorers had similar tales. Christie Palmerston recorded: The stinging bush here grows from 1 inch to 12 feet in height, having a stock similar to the sunflower. Its leaf in size resembles that of a pumpkin, but it is of a much darker green. It is shaped somewhat like a heart but rather more pointed, with a sour wrinkled-looking bearded surface. Its power of pricking is so keen that the slightest contact with those airy heated tongues forces its poisonous notice on one’s feelings, and this cannot be erased for weeks, sometimes months, and from the memory never. It bears a small pinkish-coloured fruit like a dwarfed grape. Our experience with the precipitous features of these creeks sufficiently proves that no satisfactory exploration can be accomplished with our present supply of provisions. Our wardrobe, moreover, is reduced to a state that excites laughter. Trousers patched with pieces of red and white blanket give us a harlequinish appearance. Our feet are in pitiable condition … (cited in Savage 1989).
Dendrocnide moroides (female flowers and immature fruit).
The flowers of the Stinging Tree, which are small and insignificant amid the green foliage, produce attractive rope-like clusters of berries. Although the fruit are said to be edible they are best avoided. The mere act of retrieving them can result in
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are often almost devoid of hairs. We have tossed clusters in a bag and even in the hands to break the few hairs present and have then eaten the crisp, acid fruit with enjoyment. It should be emphasized that stinging tree fruits should never be placed in the mouth until they have been carefully examined for stinging hairs, and until they have been given an opportunity of demonstrating any unfriendliness on some other part of the body.’ The fruit of Dendrocnide excelsa and D. moroides, however, should be strictly avoided. There are reports of incidents resulting in severe painful swelling of the mouth and tongue – which can seriously affect breathing, with the potential to cause asphyxiation.
Dendrocnide moroides: ripe fruit.
serious injury. Due to variations in the toxicity of the different species, this bush tucker is simply not safe for experimentation. The fruit has been described as having a crisp acid character, although the flavour differs substantially between species (Low 1992; Cribb & Cribb 1980). In Wild Food in Australia Alan and Joan Cribb commented: ‘Dendrocnide photinophylla has shiny leaves, in some cases with only a few stinging hairs, and its fruits
There are reports of Stinging Trees being a hazard if grown in hot-house cultivation. Allergic-type reactions are not uncommon due to the trees’ habit of constantly shedding stinging hairs. This not only involves accidental skin contact – inhalation of the hairs can cause substantial distress (Hurley 2000). In the early days men clearing tracks through the forest truly dreaded any encounter with the plant. Exposure to the fine hairs from the dead leaves was a serious work hazard that could result in severe irritation of the eyes, throat and mouth. Slashing through the undergrowth was particularly perilous due to the risk of accidental inhalation – making heavy gloves and respirators (and today anti-histamine tablets as well) regular safety precautions (Everist 1981). There appears to be little diminution of toxicity over time. Studies have shown that the toxic principles were not destroyed by either heat (boiling) or drying. Even after being in storage for almost five decades, dried leaf fragments have remained capable of producing a severe reaction upon skin contact. The Director of the Lake Burrendong Arboretum (western New South Wales), George Althofer, described one particularly memorable incident of inadvertent contact with a stored sample of Dendrocnide excelsa: ‘I only just touched it and it took at least five days to get rid of it. Every time I became hot it was agonizing pain. I can quite understand people being driven mad by it. The pain! Just one or two hairs had stung me, and I think it was only dry hairs because I didn’t actually handle them! They must have been blown onto me somehow
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or another’ (quoted in Lassack & McCarthy 1992). The search to identify the poisonous principles of the genus has taken decades. Even today, the full chemical explanation of the toxin’s activity remains incomplete. The initial investigations began in 1888 when Dr TL Bancroft detailed his observations in the Transactions of the Intercolonial Medical Congress. The genus Laportea has some interest to the pharmacologists, inasmuch as after being nettled, one is reminded of the fact for several days, and in exceptional cases for weeks, whenever the nettled part is wet. Upon touching water, there is produced a sudden severe pain, it is only momentary however. If the hand be the part nettled, the secondary pain starts in the spot nettled, and runs up the arm and down the corresponding side. No explanation has ever, as far as I am aware, been given to account for the secondary pain. A juice made by pounding the green leaves in a mortar gave no decided reaction with litmus paper; it was tasteless, and when injected into frogs, had no action upon them. If the stinging hairs be carefully examined, and the tops shaved off with a razor, a few will be seen to contain a minute quantity of fluid, so small a speck is it, however, that even with the microscope it is impossible to test its reaction with litmus (quoted in Maiden 1900c).
A Matter of Variable Potency
Dendrocnide moroides.
There can be considerable variation in potency of different species, a trait that has been noted in both overseas and Australian plants. The native Giant Stinging Tree, Dendrocnide excelsa, which can grow to impressive proportions in the forest (around 40
metres) has a very painful reputation. However, the tropical rainforest Stinging Tree has even more virulent activity. This is a smaller shrubby species, Dendrocnide moroides, from northern Queensland, that is said to be the most painful of the native species. The sting of D. cordifolia, which shares the same habitat, is regarded as being a little less intense (Hurley 2000). Even so, the effects of the latter should not be underestimated: ‘All parts of this species inflict a painful sting which can last for months. If someone receives a significant sting over a wide area of a limb, as a result of being hit hard by the plant, little or no sleep will be obtained the first night following the sting. Major stings cause the affected tissue to exude lymph and pains are experienced in lymph glands in the armpit or groin. Working among plants and disturbing them cause fits of sneezing and copious production of mucus from the nasal membrane’ (Centre for Australian National Biodiversity Research 2010). The rare north Queensland Dendrocnide corallodesme has stinging hairs only on the midrib of the underside of the leaf, which are therefore less likely to be available for contact. However, because it does not look like a Stinging Tree its toxicity can be underestimated: ‘This species can only be described as sneaky or well camouflaged as it looks innocuous and quite unlike the more common species of Dendrocnide’. The leaves do not have the distinctive heart shape of D. moroides, and could easily be mistaken for other rainforest plants. The sting of D. photinophylla is reputed to be substantially less painful: ‘The leaves and twigs of this species inflict a significant sting but the effect is not as bad as that of D. moroides or D. cordifolia and does not last very long. Still a plant to be avoided’ (Centre for Australian National Biodiversity Research 2010). Similar variability in toxicity has been noted in closely related Asian species. The Indian Laportea crenulata gained a reputation for being one of the most potent of the stinging nettles, producing severe contact dermatitis: ‘The stinging hairs on the plant are known to cause a severe degree of contact dermatitis and the plant is considered to
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be one of the strongest stinging nettles found in India. The sting is particularly powerful during the flowering season when it is said to bring on violent sneezing, sleepiness and fever’. These allergic reactions to the plant were so prevalent it acquired the names ‘Fever Nettle’ and ‘Devil Nettle’ (Satyavati 1987). In his review of plants of peninsular Malaysia, Henry Burkill mentioned that a rare species, Laportea pustulosa [Dendrocnide sinuata] was regarded as being more potent than Laportea stimulans: ‘The stinging hairs [trichomes] have their cell-walls loaded with silica and contain a sap which acts on the nerve-endings in the human skin; when a hair penetrates the skin both the siliceous tip and the sap remain in the puncture and produce irritation, that due to the silica lasting a long time. What the irritant liquid is, remains uncertain but probably rather than being formic acid as was believed, it is some albuminous poison.’ A local palliative was the application of lime to the skin. Although this species was utilised as a dart poison and put in food as a toxic additive, its usefulness in the latter was debatable: ‘in a mixture used criminally in food it is served fried, but it would seem useless; not unnaturally the Malays think it is useful for scaring away evil spirits’ (Burkill 1935). It would appear that it required a certain method of administration (via a puncture wound) to ensure the most effective administration of the toxin. Originally it was thought that a sap containing concentrated formic and acetic acids was responsible for the painful reaction, but this hypothesis was later overturned. The full explanation is far more complicated. The stinging hairs contain acetylcholine, histamine and 5-hydroxytryptamine (serotonin) which, no doubt, contribute to their irritable reaction. However, a very chemically stable neurotoxin is the prime suspect for the intense pain. The delivery mechanism also contributes substantially to the reaction. The leaf ’s stinging hairs, which have their cell walls loaded with silica (which is not readily biodegradable), contain a sap that acts on nerve-endings in the human skin. The
shaft penetrates the skin to allow both the siliceous tip (which readily breaks off) and the sap, to remain in the puncture – thereby facilitating the extreme irritation that causes resultant sweating, dilation of the arterioles, and piloerection (erection of the hairs at the affected site) (Seawright 1989; Everist 1981). The minute silicon needles (trichomes12) ensure maximum toxin contact with a minimum chance of the injection being dislodged or disintegrating. In 1970 two agents were isolated that could cause painful reactions. Even though the toxic peptide moroidin was later described chemically, ‘other even more toxic, components remain to be characterised’ (Seawright 1989; Leung 1986; Oelrichs & Robertson 1970). Investigations continue to evaluate the chemistry of these toxic compounds (Khan 2000). 12 The stinging trichomes can vary from different plants. Their structures alter according to plant species and genera. For example, the trichomes of Dendrocnide meyeniana are shorter, with a higher density, than those found on Girardinia diversifolia, another urticaceous species that is used for fibre production (Fu 2003).
Stephanotic acid from stem extracts of Madagascar Jasmine, Stephanotis floribunda (Apocynaceae) is chemically related to the toxin moroidin. Various peptides (celogentins) have been isolated from the seeds of a totally unrelated plant, Celosia argentea (Amaranthaceae), with chemical similarities. Some of these compounds, including moroidin, have shown antimitotic activity – which is of interest for anticancer drug development (Kobayashi 2001; Morita 2000; Yoshikawa 2000).
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The foliage of Stinging Tree plants found within the rainforest confines can have a dilapidated moth-eaten appearance. The resident insects are obviously impervious to the toxic substances, happily feasting on the leaves. The diversity of insects that can be involved is rather extraordinary: spiders, scarab beetles, assassin bugs, sapsuckers, leafhoppers, katydids, mites, green ants and even snails, lizards and the odd frog. Small moths (Prorodes mimica) and shiny greenblack beetles (Prasyptera mastersi) have a particular fancy for the leaves – as does the Red-legged Pademelon, shown below. (Hurley 2000).
Red-legged Pademelon, Thylogale stigmatica. (Courtesy: Bob Lewis, flickr)
Keith Williams, author of Native Plants of Queensland, had the misfortune to have a close Stinging Tree encounter when he fell into a clump of bushes in 1982. This triggered a well-remembered sequence of events that illustrates exactly how difficult it is to find an effective treatment. He described the clinical symptoms in some detail:
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The walk about 3-4 kilometres back to camp was indescribable. I was forced to rest on a number of occasions. Eventually camp was in sight and how thankful I was to see it. By now it was painful to walk and the gear I had to carry was no help. The temperature of my arms seemed to rise … and they were very much inflamed. The areas were immediately shaved as I had heard that the stinging hairs were of silica and could further penetrate if rubbed by contact with clothing. There was no relief and the pain was getting worse. Vinegar was applied with little result other than to increase the intensity of the pain for a time. After discarding this treatment I alternated treatment by wrapping my arms in a blanket and then bathing them in the cold water of the creek. Both these treatments gave a little relief for short periods. That night was a sleepless one as I spent most of it walking the road and keeping up the warm and cold treatments. At last the pain was almost too much to bear and I spent the hours till daylight sitting on the creek bank keeping up the bathing with the cold water. In the morning the heat from the cooking fire intensified the pain and prevented me from preparing breakfast. We packed up in a hurry and set out for Atherton and a doctor.
Keith was given tablets to take (probably antihistamines), but the application of a commercial product named Stingose gave more immediate relief. It was applied every time the pain flared up although, unfortunately, the area had to be washed before every application – a procedure that caused extreme distress: ‘In spite of these treatments my arms were a continual source of pain and any change of temperature from any source or any contact with water could be guaranteed to restart the pain from the little relief I was getting. Keeping up the application of the ‘stingose’ was the only means of getting any relief, even if the respite was of short duration. This continued until I arrived home by the middle of November.’ Achieving complete resolution is often a prolonged process, as Keith found out. Meanwhile he became extraordinarily wary of anything that would once again trigger more suffering. ‘As the days, weeks and finally months passed my condition continued to improve. It was the longest healing process that I have experienced.’ It was seven months before most of the pain resolved although, even then, the condition occasionally flared up.
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In a letter to Joseph Maiden, Mr Crawford of Moona Plains (New South Wales) mentioned another remedy: ‘I do not know if you are aware of it, but the best cure for the sting of the leaf [Dendrocnide excelsa] is a piece of the bark (from a young plant is most convenient, chewed up and rubbed on the spot); it is as if you wiped the pain away with a cloth; it has the same effect used for the sting of the large nettle found in the shrubs – a native nettle [Urtica incisa] I think’ (Maiden 1900b). A report in the Newsletter of the Friends of the Botanic Gardens in Cairns (December 1998) gave an equally hopeful report of a remedy. It described the effectiveness of the preparation of root-bark from the Stinging Tree itself. Apparently the relief was almost instantaneous: ‘A member of the party dug up a piece of the root from the stinging tree and rubbed the bark from the root on the sting. 12 seconds later the pain eased off and 17 seconds later the pain was completely gone! 30 seconds later the Flying Doctor was called off.’ Interestingly, a very similar recommendation was recorded in the Queensland Agricultural Journal of 1 May 1899, in a letter from Mr George Patullo: ‘When stung by a nettle, bruise the leaves and rub them on the part stung; or if by stinging trees – there are two kinds, the large-leaved and the smooth, dark, glossy, green-leaved – cut a piece from the bark and rub the under parts with the juice on the place where stung, and great relief will ensue.’ Mr Patullo was undoubtedly referring to southern species of the tree, as the northern Stinging Trees tend to be shrubs from which it can be extremely difficult to harvest the bark. While it is likely that other native remedies may have been useful, these treatments do not appear to have been recorded.
Rumours of an Antidote
A widely reported remedy for Stinging Tree injuries involved the use of a milky acrid juice from the stem of the Cunjevoi (Alocasia macrorrhizos). This was said to give instant relief – a rumour that persisted from the earliest days of the country’s exploration. Indeed Carl Lumholtz recorded: ‘Still, I found the feat of this nettle to be exaggerated. If you at once put on some of the juice of the plant called Colocasia macrorhiza, which resembles an arum, and which is always
Giant Stinging Tree, Dendrocnide excelsa, and Cunjevoi, Alocasia brisbanensis. (Courtesy: Cgoodwin, Wikimedia Commons project)
found growing near the nettle, the pain is soothed and the effect of the poison neutralised. This sharp white juice, which is itself poisonous, produces a violent smarting pain where the skin is thin, as for instance on the lips. It is a remarkable fact that the antidote to this poisonous nettle always grows in its immediate vicinity.’ It seems that he was not writing from personal experience as this ‘claim to fame’ was viewed by others with a great deal of cynicism. Despite its renown many found the Cunjevoi virtually useless. Christie Palmerston was clearly disillusioned by the antidote’s reputation: ‘We spent the whole day climbing peaks and crossing the rugged sources of creeks, wrapped in the most frizzled manner by masses of thorny vines and stinging bushes … For the three following days we passed over similar country, occasionally coming across traces
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of aborigines, and nearly stung to death by the stinging bush, which attacked our bare legs in a frightful manner. A plant grows alongside which is said to be an antidote but we did not find it so’ (quoted in Savage 1989). Numerous other antidotes have been proposed. They range from shaving the area, to the application of mud, lime, juice of an onion or the Calamondin (Citrus mitis), condensed milk, adhesive tape (which is then torn off in attempt to remove embedded stinging hairs), spirits of salts, sodium bicarbonate swabs, various oils, etc. Even the sap of the stinging tree itself has been considered useful. Dettol was reported to give some relief by an army ambulance field unit. Unfortunately the effectiveness of these remedies is not guaranteed. The Kuku-Yalanji tribe of Mossman Gorge believe that the Stinging Tree provides its own cure. They smeared the juice of squashed berries over the painful area and let it set. This was then scraped off with the blade of a knife that (hopefully) removed most of the stinging hairs (Roberts, Fisher & Gibson 1995). However, if the stinging hair is cut off, this leaves it embedded in the skin. The ambulance service now employs plastic skin, which is ripped off, pulling the needle-like toxic darts out of the skin – although there can be substantial variability in the efficacy of the treatment. Success with the application of dilute hydrochloric acid (1:8 dilution) has also been reported – in combination with manual removal of the hairs first with an application of hot wax if the sting exposure is significant. There are also suggestions that the application of clay has a detoxicant and neutralising effect on the toxin. Personally, I have used Urtica Cream with great success in mild cases. Urtica urens herbal cream. (Courtesy: Martin & Pleasance, www.mandp.com.au)
Caterpillar Capers
Processionary Caterpillar nest and adult ‘Bag Shelter’ Moth (Ochrogaster lunifer). The native Processionary Caterpillar is commonly found on species of Grevillea, Eucalyptus and Acacia, although not limited to these trees. They nest in large numbers in a cosy bag-like shelter, emerging in a long processionary line at night to feed. (Image of moth courtesy: Donald Hobern, CSIRO)
There is another stinging hazard of the rainforest of interest. Processionary (or Procession) Caterpillars are the grubs of a ‘Bag Shelter’ Moth (Ochrogaster lunifer). Their name comes from the organised manner in which they ‘move house’ after their local food supplies are exhausted. Forming a nose-to-tail procession the colony undertakes a journey to find an acceptable site to set up camp again. This migration can be a potential cause of consternation and discomfort during the night for unsuspecting campers if their paths happen to cross. Indeed, these caterpillars are known as ‘itchy grubs’ for a very good reason – as they are covered in multitudinous irritant hairs. Unlike some other caterpillars and grubs, they were not utilised by Aboriginal people as food unless there was great need. The stinging hairs, even if they were singed off, could still have irritant effects. In 1896 Walter Froggatt, the entomologist, gave a detailed description of the caterpillars’ residence in the Proceedings of the Linnean Society of New South Wales:
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When they have served their purpose, and are abandoned by the full grown caterpillars, they will remain for a considerable time a solid mass of skins and castings compact and firm, protected by the strong silken coverings. These curious structures are woven round the twigs by the gregarious larvae of several different species of moths belonging to the genus Teara (Family Liparidae). They are constructed for shelter during the day, and are not used for pupating purposes. Hiding therein during the day, the caterpillars issue forth at dusk, feeding all night over the tree and returning to cover at daybreak. When moving about they travel in procession. The first large nest I came across I carried home, and was very much surprised next morning to see a string of large hairy caterpillars stretching right across the foot of the tent; they had emerged from the nest in the night, but were unable to find their way back.
Mr Froggatt was fascinated by their habits and started a collection: ‘I have, during the last season, been fortunate in breeding one of our largest species.’ His observations continued for some months: About fifty specimens of nearly mature larvae were collected and placed in a large glass jar in the Museum, where they remained huddled together in a hairy mass, unless disturbed, when they would all set off in a procession round the walls of their prison, one behind the other, often keeping it up for hours together. In about a fortnight they began to burrow into the loose sand at the bottom of the jar, constructing soft felted cocoons out of the hairs upon their bodies. The pupae were stout and short, smooth, shining, of a reddish-brown colour, with the anterior portion small and the tip of the abdomen curved upwards. The first moths emerged about the end of September, and the last two months later; but from the fifty specimens not more than eight moths were obtained.
These were identified as Teara contraria (now Ochrogaster lunifer). The vacated bag-shelter is left full of irritant silken hairs, faecal pellets and old larval skins. However, despite its grubby condition, it can provide a versatile bandage. Aboriginal people harvested the old bag-shelter for use as a protective dressing for wounds, discarding the inner layer of the nest during the process. Cleaning it would
have been a painstaking and unpleasant task due to the highly irritant caterpillar hairs, which can be responsible for moderate to severe allergy-type reactions with symptoms of swelling, redness, oedema and severe itching (pruritus). Despite this, when cleaned, the silk made an excellent dressing for burns. Even severe injuries were reputed to heal well with its use, although sometimes it was presoaked with breastmilk prior to its application. There is, however, a rather sinister side to the use of the caterpillar nest involving the selective harvest of irritant hairs, which were deployed in a highly destructive manner. There is a (possibly apocryphal) story that tells of a victim who, after being punched in the stomach, automatically inhaled the fine hairs thrown at him by his assailant. Swelling of the throat was immediate and death occurred from asphyxiation. The throat oedema soon disappeared, leaving behind an unexplained death (Latz 1996; Barr 1988, 1993; Levitt 1981). No details are given regarding how the assailant fared when he used his irritant weapon. It is difficult to believe that the deliberate handling (or ‘blowing’) of such an irritant agent is a strategy that would be devoid of some serious pitfalls.
Medicinal Nettles
The leaves of the Stinging Tree were once used by Aborigines to cure rheumatism by inflicting stings on the affected site – a cure that sounds more like inflicting pain than easing it. It appears that this practice is rooted in ancient traditions that are remarkably similar to the use of the Stinging Nettle (Urtica urens) in Europe. Inflicting nettle stimulation to painful sites was said to improve blood flow and ultimately ease the pain. Somewhat less comprehensible was the ancient Roman habit (for males) of flagellation of the ‘private parts’ with nettles to achieve an erection. Certainly a more considerate analgesic remedy was an Australian Aboriginal preparation of the pounded and boiled leaves to make a treacle-like mass, which was applied locally. In 1951 a Dr Winterbotham recorded that the Yinniburra tribe, from the Sunshine Coast region of Queensland, utilised the leaves of the Stinging Tree, gympie gympie, which were first
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suspended over a fire to burn away the fine irritant hairs. They were ‘mixed into a paste with water – the paste was then spread over the shoulders where the tribal cuts were to be made during initiation. The effect was to deaden the pain’ (Colliver 1972). A fascinating account of the use of the Giant Stinging Tree was recorded by Mr Crawford in a letter to JH Maiden: The bark is … said to have been used by the blacks in the olden times for the cure of rheumatism, also for ‘giggle giggle’, a skin complaint, also for mange in their dogs. I can remember one man, said to have been cured of rheumatism, and said to have been so bad that he could only crawl round the room, supporting himself by the wall. The blacks took him in hand, stripped him, laid him on a sheet of bark, rubbing him with the young leaves and bark of the Laportea, pounded up and boiled until it was of the consistency of treacle. It is said that they almost rubbed the man’s skin off, but they cured the patient (Maiden 1900b).
Many therapeutic recommendations for the use of Stinging Tree have changed little from those known a century ago. Dendrocnide decumana, a species of southern Asia and Malesia (ranging from Borneo, Sulawesi and the Moluccas to Papua New Guinea), is still utilised in tribal medicine today. Beatrice Blackwood wrote in 1889: ‘For internal pain the usual treatment is to make certain leaves hot over the fire and press them on the skin at the locus of the pain. Sometimes the leaves are rubbed over the skin; other prescriptions call for them to be chewed and swallowed. Unfortunately, very few of these are determinable. For pain following childbirth the leaves of a species of nettle (Laportea decumana) are rubbed over the abdomen, the sting apparently acts as a counter irritant.’ In the PNG Highlands, around Morobe Province, this species continues to be recommended for alleviating aches and pains, the leaves (stinging hairs included) simply rubbed onto the body. The area swells up and the muscles relax. Popular as a remedy for muscular fatigue, the nettle is often massaged directly on the leg muscles to give relief after walking long distances or after enduring the travails of hunting parties. Other recommendations include the treatment of headache, bruising or intestinal pain. In some areas the remedy has been employed for
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conditions as diverse as splenic enlargement, stomach ache, abdominal pain following birth, or rubbed on the chest for asthma (Woodley 1991). It is interesting to note the resemblance of these practices to that of the old world Stinging Nettle (Urtica dioica), which has an analgesic reputation that is centuries old. One old nettle ointment recipe utilised a mixture of chopped nettles, salt, vinegar and pure lard, which was spread on a piece of brown paper and applied to painful areas. Some traditions appear to survive to this day, as the following recent account illustrates. A treatment for a frozen shoulder involved green nettles put directly on the skin and left for several days. Apparently, once the discomfort of the remedy was overcome, the shoulder was cured: ‘A friend, now over 80 years old, who came from Fife recalled being told how her father was cured of a frozen shoulder when nettles were put on the bare skin of the shoulder area and kept on for, probably, several days. When the nettles were removed, and despite the blisters caused by them and the pain suffered, the man was cured, for all time [Edinburgh, January 1992]’ (Vickery 1995).
An Urticant Remedy In Australia the various Nettles can be difficult to distinguish. At the sunlit edge of the rainforest and creeks the native Scrub Nettle (Urtica incisa) can be found, while the introduced weedy Nettle (U. urens) is familiar around farms and waste places. Nettle leaves were eaten by Aboriginal Flowering Stinging Nettle. people. They contain a valuable range of minerals and amino acids, and are particularly rich in vitamin C and β-carotene. Nettles have
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long been used to treat rheumatic pains and sprains; for example, they ‘beat the affected parts with a bunch of leaves to cause a nettle rash’ or ‘for sprains dip the leaf into hot water, chop into small pieces then boil in water and use decoction to bathe affected part’. A leaf poultice was similarly deployed (Webb 1969). Boiling the leaves abolishes their stinging ability and therefore the use of a tea, wash or poultice would be a less painful experience than the traditional practice of ‘flogging’ with nettles (urtication). It is interesting that urtication was once widely used in European medicine for the treatment of chronic rheumatism, lethargy, coma and paralysis. The whole plant is covered in sharp, hollow, stinging hairs that contain an irritant fluid. Touching the spines breaks the top allowing the fluid to be promptly injected into the skin – resulting in irritation and inflammation. The genus name Urtica comes from the Latin urere, which describes these urticant hairs.
Stinging hairs (trichomes) of Urtica dioica. (Courtesy: Jerome Prohaska, Wikimedia Commons CCA-SA, Copyleft Free Art Licence)
In Australia Dr Wojciech Kielczynski has been researching the leaf tincture of the Giant Stinging Tree (Dendrocnide excelsa). In arthritis treatments the tincture was taken both internally and applied externally in various combinations (with or without other herbal remedies). Patients who were treated with an anti-inflammatory herbal preparation (a mixture of Harpagophytum, Cimicifuga, Zanthoxylum and Betula), had better results when Dendrocnide excelsa was added
to the mixture. There was a marked reduction in their reliance on conventional medication. The external use of the tincture also greatly helped pain relief – and could ‘relieve the ache of stinging nettle pain with the application of the bark of stinging nettle tree with close to 100% success’. Although the study was small it gives an interesting insight into the potential of this plant as an analgesic in arthritic disorders (Kielczynski 1997). However, Dr Kielczynski commented that he had ‘never used Dendrocnide alone because of lack of steady supply. There is a possibility that a tree that grows in Victoria is not as efficacious as that from the tropics, but the result obtained by addition of that herb to my anti-arthritic mixes was impressive’.
A Spiritual Dimension to Healing
Many cultures believe in the ability of ‘powerful plants’ to enter other realms of the spirit. This spiritual dimension is intimately intertwined with their curing abilities: ‘Dendrocnide and ginger are regarded as powerful substances which are beneficial when used alone or in combination with others. The pain caused by nettles is said to drive out the pain from illness’ (Johannes 1975). The Stinging Tree has a potent ability to produce pain, which was linked to the perception of an equally strong spiritual or protective capability. A belief in the practice of sorcery has been strong in many areas of Australia, Oceania and Papua New Guinea – and the plants used to counteract ‘strong magic’ were often regarded as valuable healing remedies. In Papua New Guinea, where the medicine man may still be called in to treat fatigue, aches and pains that result from evil sorcery, ‘He will rub patient’s skin with leaf of a stinging nettle (of the Urticaceae family, Dendrocnide; ps’si in Bena Bena) over which he has spoken magical words’. In Malaysia the Stinging Tree was regarded as being useful to scare away evil spirits, while in the Fiji Islands it has been used in making a medicine to treat diseases attributed to evil influences (Johannes 1975). Perhaps the strangest report of the use of the Stinging Tree comes from northern Australia where in 1901 Walter Roth recorded: ‘At certain of the
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corroborees on the lower Tully River some of the blacks will chew and spit out again, the leaves of “stinging tree” [Dendrocnide]. The immediate effect is apparently a condition of frenzy, in which the individual may take violent action on his mates, or
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perhaps more commonly produce in himself a grossly disgusting perversion of the alimentary functions which enables him to eat human excreta’. The whole description seems somewhat bizarre, leaving the reason for the use of the plant open to conjecture.
Table 1.1 Medicinal uses of Stinging Trees (genera Laportea and Dendrocnide) Classified in the Stinging Nettle family (Urticaceae), the Australian Dendrocnide species were originally included in the genus Laportea. However, these plants were sufficiently different to rate a separate genus – which is also found in South-east Asia, Oceania, China and Japan. Laportea is more accurately applied to plants of American origin. In the older literature Urtica has been widely applied to numerous species in both genera. Species (distribution)
Traditional uses and investigations
Laportea aestuans (syn. Fleurya aestuans) West Indian Woodnettle, Red Stinging Nettle
Trinidad & Tobago (Lans 2007, 2006): • leaves used to make remedy for childbirth to shorten labour. • leaves used to treat diabetes. Caribbean (Honychurch 1991): • leaves mixed with oats and used for ‘stricture’ in Barbados – sometimes associated with difficulty urinating (dysuria). West Africa (Ayensu 1978): • constipation (leaf boiled); burns (slightly scorched leaves applied); dysentery (leaf enema); female confinement (leaf juice); wounds (liquid from macerated leaves with palm oil); rickets (infants: decoction used as a lotion). Trinidad, Brazil and Peru (Morton 1981): • plant decoction: taken as a diuretic. Cameroon (Jiofack 2009): • leafy stem & root decoction: anaemia, calcium, fibroids, dermatitis. Papua New Guinea (Holdsworth 1977): • Bougainville Island: root and stem bark are externally applied to sores on the soles of the feet.
Widespread in the tropics: tropical America, West Indies, tropical Africa, Madagascar, Arabia, India, Sumatra, Java, Lesser Sunda Islands
Dendrocnide amplissima (syn. Laportea amplissima) Indonesia (Sulawesi), Moluccas Laportea canadensis Canadian Woodnettle Eastern North America, from Canada to Mexico
Laportea crenulata Bangladesh, India, Sri Lanka, Malay Islands
Indonesia (Perry & Metzger 1981): • sap is bechic (for cough relief), sap squeezed from crushed bark drunk to treat sprue (a disorder involving sore throat, raw tongue and digestive problems). North America (Moerman 1988): • febrifuge: plant decoction for fever; • antidote: fruit decoction (with menstrual blood) to counteract pain; • emetic: root decoction to induce vomiting to neutralise a love medicine; • emotional and witchcraft: decoction to counteract loneliness because woman has left; • tuberculosis remedy: compound infusion of smashed roots; • urinary tract disorders: diuretic; root infusion for various urinary tract disorders including incontinence. Papua New Guinea (Webb 1959): • report of its use as a contraceptive, and an unidentified Dendrocnide species as an abortifacient. Bangladesh (Rana 2009): • plant: widely used for treating bleeding (from nose, mouth), excessive gas or acid in stomach, constipation, weakness, asthma, gout, mumps, whooping cough, chronic fever. • root: urinary tract infection; said to reduce susceptibility to rheumatic disorders and colds. India (L. crenulata, syn. L. stimulans; Satyavati 1987): • root juice considered useful in treating chronic fevers; • roots and leaves are applied to swellings or ‘blind’ abscesses; • seeds: used medicinally in similar manner to Coriander. Investigations Laportea crenulata (syn. L. stimulans, Satyavati 1987): • extract of the whole plant (excluding roots): diuretic activity in rats.
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• no antiviral, hypoglycaemic, anticancer, cardiovascular or central nervous system responses. Urtica crenulata (Rana 2009): • methanol stem extract: analgesic (antinociceptive) activity, but not anti-inflammatory. Urtica crenulata (Rahman 2010; Rahman 2008): • stem extract: moderate antibacterial activity against Salmonella typhi, Shigella flexneri, S. sonnei and Bacillus subtilis; • inactive against Staphylococcus aureus; • significant cytotoxic and antioxidant activity. Laportea crenulata (Khan 2008, 2007, 2007a, 2007b): • antifungal triterpene isolated from roots; • root extracts showed good antipyretic activity; • neuropharmacological investigations for CNS activity: dose-dependent stimulant effect Dendrocnide decumana (syns Laportea decumana, L. armata; Urtica decumana) Southern Borneo, Indonesia (Sulawesi) and New Guinea
Dendrocnide harveyi (syns Laportea harveyi; Dendrocnide milnei) Pacific Islands: Samoa, Fiji
Laportea interrupta (syns Fleurya interrupta; Urtica interrupta) African Congo, South Africa, Abyssinia, India, Sri Lanka, Japan, China, through to the Pacific Islands
Papua New Guinea (Woodley 1991; Holdsworth 1993, 1996; Holdsworth & Damas 1986): • widespread use for pain and fatigue: leaf rubbed on forehead for headache, or on body for pain. • a skin fungus called sipoma is also treated by rubbing the leaves directly onto the area leaves: rubbed onto the back, shoulders or legs to relieve muscle pains and fatigue, on stomach for stomach ache and on chest of asthma sufferer PNG Highlands: fresh young leaves are eaten with sweet potato or taro for intestinal pains. PNG (Blackwood 1889): • pain following childbirth: the leaves of a species of nettle (Laportea decumana) are rubbed over the abdomen, the sting apparently acts as a counter irritant. Amboina (Perry & Metzger 1981): • Rumphius recorded that the nettle leaves (L. decumana) were struck or stroked over an area if a person felt uncomfortably stiff or rigid following fatigue or itch; numerous lumps appeared that disappeared within 30 mins, and ‘one feels considerably relieved’. • A similar custom exists in New Guinea: lower legs of individuals climbing to higher altitudes are stroked with bundles of leaves to stimulate circulation and relieve chill when weather is bad. Fiji (Cambie 1986): • bark said to provide good cure for the sting of its own nettle-like leaves; decoction of bark used for treating urinary and menstrual disorders; bark also used for infected testes and with barks of other plants for arthritis (including rheumatoid conditions). Fiji (Weiner 1985): • preparation made from scrapings of bark used to treat an illness described as ‘pain in the lungs with vomiting of blood (possibly tuberculosis); liquid squeezed from leaves given to cure fits in children, ‘sickness after birth’, and to aid expulsion of afterbirth; stem scraped and pressed to produce a fluid given for ‘stomach swollen but not pregnant’ (false pregnancy). Thailand (Anderson 1993): • infusion or poultice: local application to fungal infections which are particularly prevalent in rice-field workers. PNG, Reite (Nombo & Leach 2010): • used to mend broken bones: heat area of break and cover with nettle, tie in place with split bamboo to hold bone in place (magic incantation accompanies treatment). PNG (Holdsworth 1987): • Papuan coast: L. interrupta and Phyllantus niruri plants are boiled together and the solution drunk to relieve whooping cough. PNG (Holdsworth & Damas 1986): • leaves of small nettle rubbed onto aching head for relief twice daily; similar treatment stimulates tired muscles; L. decumana used for same problem in many regions. Southeast Asia (Perry & Metzger 1981): • Indochina: leaves crushed with water to make paste dressing for well-cleaned ulcers • New Guinea (Tami Islands): painful spot beaten with this weed before performing venesection.
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Philippines (De Padua 1977–83; Quisumbing 1951): • leaves: applied to carbuncles; • root: decoction taken as a diuretic, and also prescribed as a remedy for coughs and asthma. Solomon Islands (northwest)(Blackwood 1889): • leaves used at puberty rites; flowers to treat sores on soles of feet. Dendrocnide latifolia
Solomon Islands, Guadalcanal (Perry & Metzger 1981): • the boiled leaf applied to itchy skin conditions.
New Guinea, Bougainville, Pacific Islands (Solomon Islands, Vanuatu, New Caledonia, Marianna Islands, New Hebrides) Dendrocnide meyeniana (syns Laportea gaudichaudiana, L. batanensis; L. mindanaensis; L. pterostigma; L. meyeniana; Urtica meyeniana) Poisonous Woodnettle China, South-east Asia, Taiwan, Philippines Laportea ovalifolia Africa
Dendrocnide stimulans (syn. Laportea stenophylla) Elephant Tree Nettle Southern China, South-east Asia (Thailand, Peninsular Malaysia), Indonesia (Sumatra, Java, Sulaweisi, Borneo), Taiwan, Moluccas, Philippines
Dendrocnide sinuata (syns Laportea sinuata, L. pustulosa; Urtica ardens) India, South-east Asia, Malaysia, Indonesia (Java, Bali), New Guinea Laportea (Zhu Ma: undetermined species) Thailand
Southeast Asia (Perry & Metzger 1981): • Taiwan: D. meyeniana, L. pterostigma and L. batanensis (= L. kotoensis): pounded root and leaves applied to treat scrofula. • Philippines: the watery sap was drunk to increase the supply of breast milk; root and leaf infusion used as a diuretic in cases of urine retention. Laportea pterostigma (Satyavati 1987): • extract whole plant (excluding roots): demonstrated behavioural effects and an amphetamine activity in mice.
Cameroon (Momo 2006): • aerial parts used for the treatment of diverse illnesses: bacterial infections, headache, urinary tract infections, pneumonia, dysentery, epilepsy; • leaf decoction: diabetes mellitus. Cameroon (Jiofack 2009): • leafy stem decoction: poisoning, fontanelle, flatulence, tongue pain. Nigeria (Iffen & Usoro 2010): • leaves and tender shoots used as pot herb or vegetable in soups; antidiabetic contribution to the diet. Laportea ovalifolia (Momo 2006): • plant extract: significant antidiabetic and substantial hypolipidaemic effects. Laportea ovalifolia (Iffen & Usoro 2010): • antidiabetic (antihyperglycaemic) and antioxidant properties; • note: Stinging Nettle (Urtica dioica) has also shown antidiabetic activity. Indonesia (Leaman 1991): • sapling root baked in coals and kneaded into a dough with water, the paste is applied locally to weeping sores, or applied to ‘dry out’ the external skin of a boil and allowing it to be more easily lanced. A root poultice can be applied to the gums for treating toothache. Malay Peninsula (Burkill 1935): • pounded roots (sometimes with sulphur added) or leaves were used to poultice swellings or treat ‘blind’ abscesses. Indonesia (Perry & Metzger 1981): • sap is bechic (relieves cough). Indonesia (Hirschhorn 1983): • Laportea stimulans and L. costata: sap drunk to treat cough; also utilised as a hairwash. Indonesia (Perry & Metzger 1981): • roots with leaves of Schizostachyum blumei are boiled: decoction drunk as remedy for swollen limbs. PNG (Webb 1959): • claimed to be used as oral contraceptive in New Ireland. Indonesia (Hirschhorn 1983): • root decoction with Melocanna humilis leaves drunk to treat swollen limbs. Thailand (Wang 2003): • Chinese community: root decoction taken by mother to delay birth when premature birth threatens (‘child is in danger of being born early’).
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Nettle: A Historical Healing and Haemostatic Herb
Urtica dioica (Brännässla), from Bilder un Nordens Flora (1917–1926) by CAM Lindmans.
Nettles have a long and profligate history of medicinal use that originated in ancient times. In the first and second centuries AD, Dioscorides and Galen mentioned the use of Nettle leaves for their diuretic and laxative properties. They were utilised for treating dog bites, gangrenous wounds, swellings, easing nosebleeds and relieving menstrual distress. A vast array of other disorders, including splenic problems, bleeding conditions, pneumonia, asthma, tinea (a fungal skin infection) and mouth sores were thought to benefit from their use. These traditional uses were mentioned repeatedly over the intervening centuries. In the sixteenth and seventeenth centuries, many physicians recommended Nettle leaves as a
diuretic, an aphrodisiac, as an antihaemorrhagic and for blood purification (alterative). As a healing remedy it was highly regarded for treating wounds, allergic skin rashes and burns. It was also utilised for remedying hair loss, ‘swellings’, cancer and kidney diseases. Around the first century AD, Pliny also praised the plant as a haemostatic (which stops bleeding). This use of the herb withstood the test of time, as Maude Grieve attested in her Modern Herbal (1931): ‘As an arrester of bleeding the Nettle has few equals and a infusion of the dried herb or an alcoholic tincture made from the fresh plant, or the fresh Nettle juice itself in doses of 1 to 2 tablespoonsful is of much power inwardly for bleeding from the nose, lungs or stomach. Old writers recommended a small piece of lint, moistened with the juice, to be placed in the nostril in bad cases of nose bleeding.’ Modern investigations have confirmed the herb (primarily root extracts) possesses anti-viral, anti-haemorrhagic, astringent, anti-diarrhoeal, diuretic, immunomodulatory and wound healing properties. Nettle has demonstrated a stimulating activity on pancreatic secretion, and shows antihyperglycaemic (preventing blood sugar levels rising) and cholesterol lowering (antihyperlipidaemic) properties. It has potent anti-inflammatory and prostate-healing activities, as well as a beneficial effect on immune system function. Extracts have also shown potential in anticancer studies (antileukaemic activity). Clinical studies have shown allergic rhinitis can respond well to a herbal preparation.
• The challenges of ‘bush exploration’ and settlement were not restricted to avoiding physical floral defence strategies. There were various other forms of chemical defences that had to be dealt with – as the tale of the Canavalia Beach Beans clearly illustrates. Acquiring adequate food resources in the outlying regions of the continent was a
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serious impediment to any exploratory venture. It was therefore essential to obtain local foodstuffs wherever possible. The problem was that few of the resources were familiar and poisonous consequences always loomed as a deterrent to experimentation. The use
Rainforest at Dusk, original artwork by Peter Brooke.
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of cooking strategies to ensure the edibility of these resources meant acquiring effective skills to deal with unfamiliar foods, which was a problem that presented an entirely new challenge, although the solutions were many centuries old.
Chapter 2
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS dealing with different food items. Some overt sideeffects can be readily associated with hazardous foods. Those that result in immediate discomfort such as nausea, vomiting or diarrhoea are the easiest to deal with as the association is immediately apparent – but other, less obvious, forms of toxicity can be far more dangerous. The knowledge of how to deal with these problems can often be found embedded in traditional preparation methods. In times where kitchen appliances had to be made by hand and the pantry did not come ready stocked from a supermarket, meal preparation would have been a daily challenge that required considerable skill. Over time, trial and error led to the use of a wide range of techniques to remove or inactivate plant toxins. Toxic or bitter substances in foodstuffs usually require physical removal – and the most practical way to do this was by washing in a stream or river. There were other strategies that became individually adapted to the food under preparation. As well as washing, root crops generally required pounding or cutting, and were frequently roasted, to make them edible. Roots Riverine habitats and their environs are often good sites for procuring food. Not only are there are fish in the streams, there is a diverse range of other edibles that include yabbies, crabs, worms and various forms of fruit or seed-yielding vegetation. The Blackbean and the rainforest Entada vines produce interesting large pods that contain large starch-filled seeds. However, they require considerable processing efforts before they can be considered edible.
The various methods of food processing were developed early in the history of the culinary arts. While today the basic strategies of cooking are generally taken for granted there had to be a time, somewhere in prehistory, when man worked out the best way of
Some toxic compounds can be transformed into a less toxic chemical form by a process of fermentation. This was more commonly utilised when water was in short supply and was a popular strategy in the Pacific Island regions for the preservation of Breadfruit (Artocarpus altilis). 60
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
could also be ground and made into a smooth-textured paste useful for making bread or damper. Milling or grinding seeds was equally useful for making an edible starch or dough. There is, however, another important consideration. While it would be easy to assume that simply cooking (boiling, baking) vegetables would be enough to remove any potentially poisonous components, the level of heat exposure may be inadequate to achieve complete detoxification. Some toxic compounds are heat stable, or do not dissolve in water, making them quite difficult to eliminate. The processing strategies employed by Aborigines in Australia’s northern regions quickly captured the attention of a few early researchers. Understanding the reasons behind the exhaustive care taken with the preparation of many plants was essential for procuring food from the native flora. In 1901 Walter E. Roth, the Northern Protector of Aboriginals (1897–1905) in Queensland, wrote a detailed review of the subject in a paper entitled Food: Its Search, Capture and Preparation: ‘Amongst such processes may now be noted washing, grinding, pounding, straining and grating … Washing, which may be effected by allowing running water to percolate through a sieve, in the shape of a dillybag containing the vegetable, undoubtedly removes injurious elements (Castanospermum, Cycas) and bitter tastes (Dioscorea) … Pounding, by means of a stick or stone, alternatively with roasting, certainly removes the acrid taste of several roots (Vitis) [= Cissus] which, unless so prepared, it would be well-nigh impossible to eat.’ Even though many vegetables did not appear to have overtly toxic consequences (or they were merely a mild irritant), some form of processing was usually required to make them more appetising. The success of these ventures could vary substantially.
Rainforest Blackbeans
The impressive Blackbean or Moreton Bay Chestnut (Castanospermum australe) is a large tree that features along the Australian east coast. It ranges from northern Queensland to northern New South Wales. It was one of the early botanical discoveries in 1770 when Joseph Banks collected samples from the Endeavour River, Cooktown, in northern Queensland. The pods crack open when they fall to reveal large seeds that are
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eaten with no apparent ill effect by possums and native rodents – but humans are well advised to be wary of trying this fare without prior experience with its preparation. In the raw state the seeds contain a strong natural purgative, with distressing potential. In his authoritative text on the Poisonous Plants of Australia (1981) Selwyn Everist recorded the following account of Blackbean poisoning: ‘In 1968 three servicemen in southeast Queensland who ate small amounts of raw seeds became seriously ill within 2 hours and were admitted to hospital with symptoms of vomiting, severe abdominal pain and dizziness. All recovered overnight (Qld Herbarium Records).’
An Impressive Coastal Inhabitant
The Blackbean is a large, impressive tree that prefers riverine sites. The leaves have the interesting distinguishing feature that, when crushed, they emit an unusual aroma that resembles cucumber.
The common name Blackbean was derived from the dark colour of the wood, and the fact that the seeds were borne in large pods or ‘beans’. An early review of ‘Useful Australian Plants’ by Joseph Maiden (1894), published in the Agricultural Gazette of New South Wales, provides a good description of the tree and further details regarding the origins of the botanical name:
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Castanospermum, from the Latin castanea, a chestnut, the sweet chestnut, and spermum, a seed. The tree is confined to Australia, and in non-Australian descriptions of it the name is usually explained on the grounds that ‘the seeds are roasted like chestnuts’ ... It belongs to the natural order Leguminosae. Flowers. – They are borne on the last year’s wood, bear a general resemblance to pea-flowers, though more solid and fleshy, and in colour vary from yellow, through all stages of orange, to coral red. They are very handsome, though not available for cut flowers. Fruit. – The seeds strongly resemble the horse-chestnut of Europe, but they are usually much larger in size; and they are found in a very thick pod, almost circular in section, like a distended broad bean (Maiden 1894).
days; they are then taken out, dried in the sun, roasted upon hot stones, pounded into a coarse meal, in which state they may be kept for an indefinite period. When required for use, the meal is simply mixed with water, made into a thin cake, and baked in the usual manner. In taste, cakes prepared in this way resemble a coarse ship biscuit.’ The flour was said to be ‘neither better nor worse than many of the food starches at present consumed for food’ (Maiden 1894). However, despite the quite elaborate processing methods utilised, the Blackbean could retain some toxic potential. The records of Walter E Roth (1903) provided additional details of the meticulous processing utilised in northern Queensland. Some local variations of the process were observed: At Atherton the shells being broken, the kernels are commenced to be baked about sunrise, the covering leaves and earth being removed about mid-day. They are then cut up into very fine chips with a sharp shell etc. and at about sunset are put into a lawyer-cane dilly-bag, through which the creek water is made to percolate, and there it remains until the following morning, when it is about ready to eat. On the lower Tully River, after the beans have been gathered, the nuts are removed and placed in heaps in the ground-ovens. After covering with leaves and sand, a fire is lit on top, with the result that the nuts are practically steamed, a process occupying from a few hours up to a whole day. When removed they are sliced up very fine with a snail-shell knife, and put in dilly-bags in a running stream for quite a couple of days when they are ready. If not sliced up very fine, the bitter taste remains.
In summer, the Blackbean produces stunning displays of gold, orange and red flowers, the nectar of which is extremely tempting to flocks of parrots.
Castanospermum australe seeds provide an excellent illustration of the complex and tedious detoxification techniques that were occasionally deployed by Aboriginal people. Removing the toxins in running water, or by fermentation, was an essential step in making the seed starch edible. In 1866 a gentleman by the name of Mr Charles Moore exhibited Blackbean seeds at the Intercolonial Exhibition, Melbourne, with the following explanation of their preparation: ‘The beans are used as food by the aborigines, who prepare them by first steeping them in water from eight to ten
For this reason, even after all this effort, the result was not necessarily relished: ‘On the Bloomfield, this nut is nearly always obtainable … It is one of the worst foods to prepare, a long time being required to wash away the disagreeable flavour’ (Roth 1903). In 1828 the Superintendent of the Sydney Botanic Gardens, Mr Charles Fraser, undertook a trip to Brisbane with the aim of establishing a botanic garden there. He was accompanied by the botanist Allan Cunningham who at the time was working with the Royal Botanic Gardens at Kew, London. Upon discovering the Blackbean tree Fraser wrote: ‘By the natives the fruit is eaten on all occasions; it has, when roasted, the flavour of a Spanish chestnut, and I have been assured by Europeans who have subsisted on
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
it exclusively for two days, that no other unpleasant effects were the result other than a slight pain in the bowels, and that only when it was eaten raw’ (Maiden 1900a). Despite these optimistic assertions, experiments by many early settlers were to prove otherwise. Over the intervening decades, the unwary continued to suffer from underestimating the toxicity of this food source.
A Stock Toxin
Blackbean seeds, which float well, migrate easily to the ocean from their riverine habitat and are frequently seen strewn along the tropical northern beaches. The seeds are extremely resilient and have undertaken some remarkable sea journeys. They have been found washed ashore on the New Zealand coastline, an ambitious journey across the Tasman Sea. The buoyant empty pods have also provided ready-made toy boats.
The fact that stock animals sampling Blackbean seeds could suffer severely from gastrointestinal distress has not endeared the tree to the farmers of the country. Cases of gastroenteritis have been frequently reported in cattle and horses. Selwyn Everist mentioned field observations that showed: ‘[the most] consistent symptom is severe scouring often accompanied by emaciation, debility, laboured breathing, drooping head, and ears; dull/ staring eyes; hard, harsh and dry coat; constant micturition; at autopsy severe inflammation of stomach and intestinal tract’. This description is very similar to that reported by Joseph Maiden 80 years previously (Maiden 1894). For this reason ‘stockowners have long waged war against it,
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because the “beans,” if eaten by cattle and horses, produce acute indigestion, which sometimes results in death’. Maiden commented that cattle seemed to become inordinately fond of the leaves: ‘The beans kill the stock, owing to their highly indigestible character, the indigestible portion in time forming a ball in the stomach. The leaves also are found to be injurious, and animals which take to eating them become very fond of them, and when taken away return long distances to these trees, and according to some accounts become affected similarly to animals which eat the Darling Pea1, and, if not carefully looked after, they will pine away and die.’ At the time Blackbean poisoning had been the cause of numerous fatalities in the Richmond River area. During the drought cattle were attracted to the bright green immature beans lying under the trees. The stock that survived suffered severe purging. In addition, while horses dining on the toxic fare exhibited no symptoms, they died soon after. 1 The Darling or Poison Peas refer to the genus Swainsona.
Blackbean has had limited medicinal value, although its toxic properties usually seem to have surpassed its usefulness. The inner white bark had a particularly potent poisonous reputation that appealed to the vindictive side of some individuals. A note by Len Webb mentioned its use ‘boiled in water to make a poisonous solution which was allegedly put in the victim’s food or drink’ (Webb 1969). Investigations have isolated a number of water-soluble alkaloids, notably castanospermine, which have shown antiviral, anticancer, anti-inflammatory and possible pesticidal activity. Although these compounds are highly toxic, they have played an important role in biochemical investigations into viral disorders such as HIV-AIDS (Che 1991). The bark of the tree has been utilised as an antibacterial remedy for the treatment of skin problems and a natural bandage for wrapping burns. There is, however, another rather odd practice that was associated with the use of the seed at the Tully River: ‘a woman will get a man to fancy her by passing into her vulva a nut of the Castanospermum australe … or of the
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Cryptocarya bancrofti. She may place it in the position mentioned at any time, but apparently does not keep it there for very long’ (Roth 1903). Any other details regarding this custom remained unrecorded.
A Glorious Timber
Blackbean floor. (Courtesy: David Gunton, www. wideboards.com)
Blackbean has been a famous cabinet-making and furniture timber. Joseph Maiden (1896) commented that timber strongly resembled walnut: ‘It is dark-coloured, fine-grained, and takes a good polish. Very few woods can be dressed with greater facility. It shrinks in drying, though not excessively so, and it is well worthy of any attention that may be given it as regards seasoning. It is of a greasy nature and will not readily take glue. It is tough and durable. Showy figured specimens are not uncommon.’ Blackbean’s hardness and attractive grain made it popular for flooring. Although many native timbers did not live up to the claims that were made for them, Maiden’s praise of the Blackbean was effusive: I have always endeavoured to urge moderation in advocating the claims of colonial timbers, feeling sure that our timbers have received a good deal of harm from indiscriminate praise; but, having kept Black Bean under observation for a number of years, and having
caused large quantities of it to be worked up into various articles, I think very highly of it. I look upon it as scarcely inferior to walnut … Let Black Bean be felled when the sap is down, and I do not hesitate to say that it may be pitted against walnut without disgrace. Black Bean is easier to dress than even cedar; in fact it is almost perfection as regards the ease with which a surface can be got on it. It polishes readily, but the grain is inclined to rise under polish. This timber often shows a beautiful figure; planks which have the figure in bands, like the marking of an agate are really gorgeous (Maiden 1894).
Despite being a superb candidate for use as a cabinet timber, the wood was not durable if used ‘under the ground’, and this made it totally impractical for fencing or making posts. The thick white sap-wood was readily attacked by borers: ‘Insects speedily reduce it to a flour-like substance’. There was one other drawback to its use that was encountered in the milling process – the dust had serious irritant effects on the skin and mucous membranes: ‘The wood has been accused of affecting the health of workmen who handle it’ (Webb 1948).
Starch from Plants
Food-processing strategies do more than simply make various food items acceptable to the palate. Certainly some unappetising resources are made more appealing and, importantly, toxic components are often removed at the same time. In some instances, while the original reason for the processing may have been forgotten over time, the method used remains unchanged for practical reasons. Some strategies were quite complex, as the procurement of starch from tubers illustrates. The term ‘arrowroot’ has been used to describe many plant-derived edible starches. This is typically the fine starch that is useful for making baby food, pastries, puddings and to prevent milk curdling. Arrowroot is easily digestible for those convalescing after illness and has soothing demulcent properties useful for individuals suffering gastrointestinal distress. It can also help the tissue repair process following conditions
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
Bermuda or West Indian Arrowroot (Maranta arundinacea)
The tuberous root of the Bermuda Arrowroot was once used as a antidotal remedy for poisoned arrow wounds, hence the name ‘arrowroot’. It was also applied as a healing agent (vulnerary) for ulcers and other form of injury. The starch was recommended as a useful soothing application for diverse skin problems: erysipelas (an inflammatory skin condition), sunburn, wasp stings, dermatitis, or even damage due to gangrene. In the Caribbean the pounded leaves were used as a teething aid and in Trinidad the tuber starch was used as an anti-inflammatory skin poultice (Duke 1985; Honychurch 1991; Wong 1976). Indian traditions have used the rhizome (powdered) with milk for the treatment of urinary complaints and asthma (Silja 2008).
Maranta arundinacea. (Courtesy: Zélia Doneux Rebske, flickr)
Arrowroot, from the Pharmacopoeia (1967).
Martindale
Extra
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such as diarrhoea or dysentery. The plants utilised as a source of Arrowroot can vary considerably between countries (Grieve 1931). The Bermuda or West Indian Arrowroot from Maranta arundinacea has been one of the most familiar, although other species within this genus are suitable, among them M. allouya and M. nobilis from the West Indies. ‘Tous-les-mois’, another form of arrowroot starch, is sourced from Canna edulis and C. achiras. Other resources include Tahiti Arrowroot (Tacca pinnatifida), East Indian Arrowroot (Curcuma angustifolia and C. longa), Chinese Arrowroot (Nelumbo nucifera), Portland Arrowroot (Arum maculatum) and Oswego Arrowroot (Corn, Zea mays).
Cassava starch, from the Martindale Extra Pharmacopoeia (1967).
The fact that tuber crops can be a good starch resource has led to increasing interest in their commercial use. Cassava (Manihot esculenta) and Sweet Potato (Ipomoea batatas) are possibly the most familiar plants under cultivation. However, there are numerous other root tubers that can yield substantial amounts of starch, such as Yams (various Dioscorea species), Cocoyams (Xanthosoma spp.) Taro (Colocasia esculenta) and Konjac (Amorphophallus konjac and a few other species). It is only in the last couple of decades that these food plants have been accorded serious interest as starch resources.
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The Value of Starch
Cornstarch magnification. (Courtesy: Jan Homann, Wikipedia)
Starch is a product with a very ancient past that has found new roles in today’s society. It is an extraordinarily versatile item that enters into our lives in a great diversity of ways. Most of the time we remain quite unaware of its value. Starch has a ubiquitous presence that ranges from its innovative use in many common items on supermarket shelves to extensive medicinal applications. Dietary starch has attracted substantial research attention due to its potential role in cholesterol control, blood sugar regulation and obesity. Starch is a useful adhesive agent that is incorporated into many pharmaceutical and commercial applications. The food and cosmetics industries utilise starch as a neutral non-toxic binding agent. Starch has been extensively used as a thickening agent for meat products, fruit juices, snack items, bakery goods, etc. In addition, starch has been utilised in making disposable plastic-like items (cutlery, packaging), papermaking, adhesives, textiles, paints, and innumerable personal care products (disposable nappies, sanitary items, hair care, deodorants). In pharmacy, starch can be used as a binder, diluent (diluting agent) and disintegrant. There is a substantial body of work investigating the ability of starch to bind to drugs, providing different release patterns to achieve the most effective level of bioavailability. It also has a role in investigative chemistry – for instance, it has been used for the drying and separation of organic vapours.
Wheat starch granules, stained with iodine, under a light microscope. (Courtesy: Kiselov Yuri, Wikimedia Commons project)
Lotus Root: Starch and Medicine
Dried Lotus root (Nelumbo nucifera).
The Lotus (Nelumbo nucifera) is found throughout northern Australia. It creates one of the wonderful floral displays that grace inland waterways and
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billabongs. Aboriginal people utilised the fibrerich tuber as a vegetable. Lotus root (a rhizome) is a starchy tuber that grows horizontally and looks a bit like a string of sausages, the tuber swollen and pinched together at the joints. The inside is perforated with holes that run through the rhizome, giving it a characteristic appearance. The Reverend GA Stuart (1911) outlined its use as a popular Asian vegetable: ‘The root-stock is jointed and fleshy, and when cut across shows a number of cavities in the tissue, concentrically arranged, and terminating at the joints, which interrupt them at every foot or less of the length of the stock. These are boiled and sold in slices on the streets, forming a sweet, mucilaginous food, looking like sweet potato, and very much relished by the Chinese.’ The starch, which is washed from the crushed tubers, ‘answers all the purposes of the best arrow-root, and is of great value in the treatment of diarrhoea and dysentery’. The root is used medicinally both raw and cooked.2 Raw, it has an astringent flavour and cool character, and can be utilised to clam fevers, stop bleeding, for ‘heat’ in the blood and to clear blood toxins (e.g. acne, boils, carbuncles). Traditionally, this was a good first aid remedy to stop bleeding from the stomach or lungs, and was mixed with a little salt (taken daily) to prevent clot formation. Cooking (boiling) imparts a sweet flavour and warming character, making it useful as a tonic for stomach and spleen disorders. Lotus root powder has been recommended in a diverse array of conditions: for the treatment of dysentery (blend with honey, and boil to make a paste), chilblains or cracks in the foot (steamed lotus root crushed and applied locally), epistaxis (nose bleed: instil fresh lotus root juice into nose), haematemesis (vomiting blood: lotus root and base of lotus leaf simmered and taken with honey), and throat inflammation (simmered lotus root taken) (Chang 1989). 2 Hot and cold are important concepts in Chinese medicine that can dramatically alter the use of a herb. In addition, processing is well known to alter the qualities of a remedy and variations in preparation can be influential in changing the character, quality, action and toxicity of the raw material.
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In the past, toxicological considerations and laborious processing techniques limited the usefulness of many tuber crops. Recently, however, expanding markets and technological advances have led to a number of developments that require different forms of starch. This has resulted in the evaluation of various candidates to fulfil new requirements. For instance, the tubers of the Bat Plant (Tacca leontopetaloides) contain a starch whose small particle size make it suitable for textiles and fabric stiffening – an application not unlike traditional starch’s use on linen. Tacca starch can also be utilised as a disintegrant in tablet formulations, while the food industry prizes its gelatinisation characteristics (Manek 2005). Amura starch (from Tacca involucrata), which can be easily cooked and readily forms a gel, is likewise useful in food items like sauces, desserts and snacks (Zaku 2009). Tacca starch has also been investigated for use in bioadhesive drug delivery mixtures (Attama & Adikwu 1999).
Tablet Disintegrants
Natural starches can have quite different physical properties that are influenced by their water-retentive capacity and starch granule size. Starches from corn, potato and wheat were the first disintegrating agents used for making tablets. They act to promote the breakup of a tablet when exposed to moisture in the digestive system, thereby activating the release of the component drug, facilitating its absorption. Good disintegrants, which need to be effective at low concentrations, should not adversely affect the other important physical properties of the tablet (i.e. hardness, friability, compressibility). Disintegrants have the opposite effect to binding agents, although they can both be used in a single-tablet formulation to reach different target sites or timed-release drug levels. If this occurs, the type of compounds used need to be chemically compatible to avoid compromising the pharmacokinetics of the drug delivery system (Nattapulwat 2008; Ofoefule 1997). Not all starches behave in the same manner. A study of Tacca involucra starch showed it has a quicker swelling capacity than maize starch. This was of interest for use in tablets that required fast
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release of a drug, but would not be suitable for slowrelease formulations (Ofoefule 1997). Dioscorea starches are another resource of substantial interest for tablet formulation – although the properties of the starches sourced from different species can vary quite significantly (Odeku & Picker-Freyer 2009; Riley 2008). Dioscorea esculenta starch and rice starch produce tablets with a superior ‘hardness’ when compared to corn and tapioca (cassava) starches. The Dioscorea starch also had a quicker disintegrant action than the other starches (Nattapulwat 2008). Dioscorea dumetorum likewise showed good disintegrant activity that was deemed superior to that of maize starch (Ibezim 2008).
Starch, from the Martindale Extra Pharmacopoeia (1967)
The Lesser Yam or Lesser Asiatic Yam (Dioscorea esculenta) is a native of South-east Asia that has long been cultivated as a food crop. The tuber is somewhat smaller than the other common yam species, with a flavour comparable to the Sweet Potato. This species has a fairly limited medicinal reputation. The tuber decoction has been taken for kidney and rheumatic affections. In Indonesia and the Philippines the raw, finely scraped tuber was poulticed on all kinds of ‘swellings’ (e.g. swollen fingers and toes), or throat swelling (Perry & Metzger 1981). The tuber mucilage contains glucomannan, which has shown hypocholesteroaemic (lipid lowering) properties (Boban 2006).
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
Tacca: The Unique Bat Plants Intriguing Bat Plants: The Genus Tacca Taccaceae is a comparatively small family that is, rather surprisingly, among the most advanced of the world’s Angiosperms. These plants developed a very clever form of propagation with bisexual flowers that allows them to produce seed without the intervention of a pollinating agent. Tacca is a genus of tropical origins – extending from South America, Africa and Madagascar, to Asia, Australia and the Pacific Islands. Today these plants are of interest for their wonderful ornamental species, but in the past were more valued in village societies as a source of edible starchy tubers, snack fruits, and fibre for weaving purposes. Tahitian women utilised the fibre of Tacca leontopetaloides to manufacture bonnets. George Bennett (1860) recorded its preparation: ‘It [the stem] is split down, and, the inner substance having been scraped away with a shell, it is again scraped, with the addition of water, until it is well cleaned; the outer green epidermis is removed, in a similar manner, from the other side, and a fine, thick, shining white substance remains, which, dried in the sun, is ready for use.
The Black Lily (Tacca leontopetaloides) is an unusual looking long-stemmed herb topped by odd bat-shaped flowers that trail lengths of whisker-like tendrils from which numerous drooping seed heads eventually develop. The herb is found along the tropical Australian coastline from northern Queensland to the Northern Territory and northern Western Australia. It is a seasonal herb that disappears during the dry winter period, when it dies down, to re-emerge with the rains of the monsoon or ‘wet’ season.
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The Black Lily or Bat Plant (Tacca leontopetaloides) was known under a number of synonyms in the older literature – T. involucrata, T. pinnatifida and, possibly, T. hawaiiensis. The plant is believed to have originated in South-east Asia and travelled with human migration throughout the Pacific Islands. Its widespread use as a source of starch accounts for the name Fijian or Polynesian ‘arrowroot’. It was, however, not an easy vegetable to utilise – as Ludwig Leichhardt found out in 1847: ‘I tried several methods to render the potatoes, which we had found in the camps of the natives, eatable, but neither roasting nor boiling destroyed their sickening bitterness; at last I pounded and washed them, and procured the starch, which was entirely tasteless, but thickened rapidly in hot water like arrowroot, and was very agreeable to eat, wanting only the addition of sugar to make it delicious – at least, so we fancied.’ The description fits well with the use of the Fijian Arrowroot, Tacca leontopetaloides. There is another native species, that is likely to have been utilised in the same manner: Tacca maculata (formerly classified as T. leontopetaloides, although sometimes listed in older literature as T. pinnatifida var. or subsp. maculata or var. aconitifolia), with a limited distribution in northern Western Australia and nearby sites in the Northern Territory. Despite the difficulties it presented, the Bat Lily was one of the vegetables in widespread use on Cape York and provides a particularly good example of the lengthy preparation that could be involved in making some foods edible. While it could be particularly useful at times of communal gatherings, great care was exercised in its preparation. The tuber contained intensely bitter principles and in some areas was regarded as being too poisonous for use. Other tribes regarded it as a staple food. In the Northern Territory the tuber was cooked for 24 hours in an earth oven with ashes of Acacia auriculiformis before before being considered edible. The Round Yam (Dioscorea bulbifera) had a similar toxic reputation and, likewise, required roasting overnight (Smith 1993; Smith & Wightman 1990). Walter Roth (1901) recorded in great detail the different forms of processing to which Native Arrowroot tuber was exposed. Under the entry Tacca pinnatifida he wrote:
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Later, the starch could also be mixed with flour to make bread – although today it is rarely considered worth the trouble to undertake the extensive processing required to make it edible.
Yam tuber slices, prepared for Chinese medicinal use. On the Bloomfield etc. this tuber is baked in the ashes, mashed up, rolled in ginger-leaves, and then baked [R. Hislop]. At Red Island it is soaked, hammered, and roasted. On the Morehead and Musgrave Rivers ... the tubers are rubbed up against a rough stick (acting [like] a ‘nutmeg-grater’) into a bark-trough containing water. The mixture is next put through a ‘sieve’ formed of an infolded dilly-bag; it is squeezed through this into some fresh water contained in another trough. Here it is allowed to settle, for which some time is required, then washed once or twice, the water allowed to run off, and the remaining sediment scraped up with a shell, and then cooked in hot ashes like a ‘damper’. At Cape Grafton, the tubers are pounded between stones, put in water all day, the sediment removed and cooked on hot ashes. On the Palmer, it is prepared as on the Morehead and Musgrave; but when the white mush has settled in the final washing, the water is carefully drawn off, and the mess very gingerly poured onto some sand, which allows the fluid to percolate through. This white mess, now fairly coherent, is next taken in the hand and made a ball of. After being roasted in the ashes for some few minutes, its hardened exterior is skinned off, the (inner surface of this) peel being again put on the ashes. The ball itself is again similarly roasted, peeled and so gradually made up into something like four or five ‘pancakes’ which, after roasting, are then ready for eating. On the Pennefather River, it is scraped onto a rough piece of wattle bark, like a nutmeg scraper, into a shell. Then collected on to a thick bundle, 2–3 inches thick, of fine dead grass (sp. of Parotis and Panicum) as a strainer, and water poured on until all the cellular debris is left behind. The milky water is next allowed to settle, perhaps a day, the clear water run off, and the remaining flour then dried and carried about in a big hard ball. Then scraped off as wanted, and roasted on the hot stones like a pancake.
Bat Plant (Tacca leontopetaloides) fruit can be used as a bush snack when they ripen and turn yellow. The seeds, although edible, were often simply spat out into the bush, a habit that encouraged the plants’ regeneration along walking tracks (Smith & Wightman1990; Wightman & Andrews 1989).
Medicinally, the most popular use of Arrowroot starch was as a nutritious food for invalids and for the treatment of gastrointestinal problems such as diarrhoea or dysentery. Australian Aboriginal people also used the root starch as an antidiarrhoeal agent (Wightman & Andrews 1989). In the Pacific Islands there have been some other interesting recommendations associated with its use (Whistler 1992a, 1992b): • Fiji: the interior of the tuberous root was scraped out, then squeezed into water and applied as a wash for eye injuries. • Hawaii: the powdered starch has been applied to wounds as a haemostatic and was even used to staunch the bleeding from cutting the umbilical cord. • Cook Islands: the starch was applied to sores and burns and, because of its ability to act as a thickener, it was often added to medicines. • Niue: the crushed leaf stalk was applied locally to relieve the pain of bee and wasp stings.
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African healers have also utilised the plant (Abdel-Aziz 1990: • K enya: a liquid extract prepared from the crushed fresh tuber was taken as a vermifuge. It was said to be particularly useful against round worms. • Sudan: a tuber decoction was recommended for treating blood in the faeces (melaena), which was possibly associated with chronic parasitic infections, for example, amoebic dysentery or intestinal schistosomiasis.
The Palm-leaved Tacca (Tacca palmata) is native to western Malaysia and the Indonesian Archipelago, extending to the Philippine Islands. The wonderfully eyecatching bright orange berries have seen it gain popularity as a garden ornamental throughout the tropics. In folk medicine the plant has been widely used as a healing agent for skin problems: employed to reduce swellings, treat insect bites and snake bites, to mature boils, and as a wound healing agent. It was also applied to tumorous growths (Perry & Metzger 1981; Hirschhorn 1983).
Table 2.1 Traditional medicinal uses of the Tacca genus There are a number of Asian species that have been utilised in a similar manner to the Black Lily. Species
Medicinal uses
Tacca aspera
India (Abdel-Aziz 1990): • tubers used to treat skin diseases, leprosy, haemorrhagic diathesis (a tendency to haemorrhage); • valued as a tonic. Brunei (bin Haji Mohiddin 1992): • root infusion used as a remedy for headaches, slight fever, and as a cure for thrush (candidiasis). Chinese medicine (Tiamjan 2007): • rhizomes employed for burns, gastric ulcers, enteritis and hepatitis. Malaysia (Burkill 1935): • mashed roots poulticed on hairy caterpillar rashes. Thailand (Kitjaroennirut 2005): • used for blood pressure problems and as a sexual tonic. Malaysia (Ferrero 1994): • tubers poulticed on locally as an analgesic and anti-irritant remedy for insect bites. Philippines (Quisumbing 1951): • a paste prepared from chewed tubers taken as a tonic to prevent stomach complaints; • also used by women to treat menstrual problems. Java and Indonesia (Ferrero 1994; Hirschhorn 1983; Perry & Metzger 1981): • tuber shavings applied to snake bite, millipede stings, or poulticed on to ‘ripen’ boils or resolve pimples; • tuber slices also simply applied directly to cuts. Malaysia (Burkill 1935): • tuber scrapings used for healing wounds and treating snake bite; • the pulped stem was applied externally to umbilicus to treat stomach ache. China (Abdel-Aziz 1990): • recommended as an anti-inflammatory, analgesic and antipyretic; also utilised as a wound healing agent. Thailand (Anderson 1993): • the Lau people applied a poultice of a local Tacca species to sprains or broken bones; sometimes a cut was made in the skin to facilitate its penetration to the injury site.
Tacca bibracteata Tacca chantrieri Tacca cristata Tacca integrifolia
Tacca palmata
Tacca plantaginea
Tacca (unnamed species)
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The use of Tacca chantrieri in Chinese traditions for the treatment of burns, gastric ulcers, enteritis and hepatitis suggests that the remedy has good anti-inflammatory properties, possibly due to steroidal constituents. The rhizomes contain saponins and withanolide glucosides (e.g. chantriolides) – a point that is of interest in a chemical sense as withanolides are characteristic of the Solanaceae family. This plant belongs to a distinctly different classification, the Taccaceae (Zhang 2009; Yokosuka 2003). Tacca chantrieri has been utilised for the treatment of hypertension, and investigations have confirmed that extracts possess cardiovascular attributes: hypotensive, vasorelaxant (a relaxant effect on the vascular system) and can induce bradycardia (slowing the heartbeat). The effects were found to be complex, involving a number of different chemical constituents, including saponins and glucosides (Tiamjan 2007). Tacca integrifolia has shown similar experimental hypotensive activity (Kitjaroennirut 2005).
The White Bat Plant, Tacca integrifolia (syns T. alba, T. aspera, T. cristata, T. laevis) is a stunning South-east Asian herb with bracts (modified leaves) forming distinctive whisker-like tendrils. It has gained popularity as a tropical ornamental and naturally favours wetland areas throughout dense forests fringing the seashore. In Malaysia, a poultice of the tubers was utilised as an analgesic and anti-irritant remedy for insect bites (Ferrero 1994).
Riverine Rainforest Lianas
A Chinese herbal remedy: Tacca chantrieri
Tacca chantrieri. (Courtesy: Réginald Hulhoven, GFDL, CCA-by-SA3.0)
The Matchbox Bean (Entada phaseoloides) is an impressive forest liana found throughout northern Queensland. The vine’s distinctive seeds were familiar to early naturalists from encounters with the plant in Asia, Malesia and the Pacific Islands. The Reverend Tenison-Woods (1882) provided details of its distribution: ‘In all the coast jungle from Port Mackay to Endeavour River. The seeds also are abundantly strewn on the coral islets … This is the well known ‘Queensland Bean,’ the large seeds of which are made into match boxes. It is not peculiar to Queensland, but is found in the tropical countries of the whole world. The long distances to which the seeds can be carried without losing their germinating power will account for this.’ In the light of more recent classification changes he referred to a couple of predominant species – Entada phaseoloides and E. rheedei. The disc-like Matchbox beans, while considered edible unprocessed, have a decidedly bitter and acrid
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preparation the meal was not said to be particularly palatable. Walter Roth (1901) observed that it was a fairly undesirable form of fare that was ‘apparently only eaten when nothing else is available. The seed is first baked in the ashes, then cracked up and, inside a dilly-bag, left in running water all night’. Aboriginal people of the Herbert River (northern Queensland) refused to even consider them as a potential food.
There are around 30 species of Entada, which are normally rope-like vines that can grow to impressive proportions in the rainforest, although a few species can take the form of a tree or shrub. The genus is predominantly found in Africa, Madagascar, India, South-east Asia, Australia and the Pacific Islands. A few species range to the Americas. The most familiar of the genus would be a jungle vine known as the Matchbox Bean, Entada phaseoloides (formerly known as E. scandens, E. gigas or E. pureaetha), which is pantropical in distribution. It ranges from Africa to Madagascar, through Asia and the Philippines, into the Australian tropics.
character that does little to recommend them. They are more suitable for the production of an edible starch – but only after being ground to make a flour that was washed in running water to remove the saponin component (Watt & Breyer-Brandwijk 1962). Heating reduces the toxic potential. Notably, the seeds make good firecrackers when thrown into a fire. This makes the starch readily accessible (that is, if it hasn’t exploded all over the place). Joseph Maiden (1888) mentioned their use at Cleveland Bay, Townsville: ‘These large beans are eaten by the aboriginals. They are put into the stone oven and heated in the same way and for the same time as those of Avicennia tomentosa3; they are then pounded fine and put into a dilly-bag, and left for ten or twelve hours in water, when they are fit for use (Murrell’s testimony).’ Even after extensive 3 A mangrove plant of saltwater creeks and swamps, the fruit of which was baked by Aboriginal people in fire ashes in ground hollows until cooked.
The Matchbox Bean vine produces attractive starchy ‘beans’ that were once hollowed out for use as matchboxes. The vine retains an appreciable amount of fresh water that is readily accessible when cut – although care needs to be exercised not to destroy the plant.
The Matchbox Bean vine has a more practical use as a popular soap substitute due its saponin content. Its active foaming qualities saw it employed as a hair wash and soap throughout Southeast Asia. The preparation was relatively simple with the stem being cut into short lengths, beaten and sun-dried before storage. When needed, immersion in water furnished an easily prepared soap or shampoo. The benefits of an associated insecticidal effect would help rid the hair of lice, as well as being a useful skin wash for itching disorders such as scabies (Quisumbing 1951; Webb 1948; Burkill 1935). Henry Burkill observed: ‘Water into which it is thrown becomes reddish and will dye cotton a khaki colour. Though there is much more saponin in the bark than in the wood, the latter holds
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enough for use. The half-ripe seeds are also used for making a hair-wash in the Dutch Indies [Indonesia] … for the purpose, they are removed from the pods, beaten into a paste, and mixed with a little water. The measure of poisonousness of this saponin makes it of great service for cleaning the hair … wounds may be washed with it to advantage. For itch, in the Philippines, the affected part is washed with a decoction, and at the same time rubbed with the fibre. In this way the crust shielding the mites is removed, and in proportion to the energy of the rubbing, the good is done.’
Dream Beans
Entada rheedei seeds, South Africa, beach at Mapelane. (Courtesy: Paul Venter)
Entada rheedei, syn. E. scandens, the African Dream Herb. (Courtesy: JM Garg)
Entada rheedei, the African Dream Bean, which has a very similar appearance to E. phaseoloides4, has been confused with the latter in much of the literature. Entada rheedei shares a fairly similar distribution in Asia, the Philippines, Guam and Australia (Northern Territory, Queensland) – although it extends to India, China and Africa. Entada scandens, which is from Madagascar, was a name formerly applied to both species. Other
synonyms for Entada rheedei include E. scandens var. aequilatera, E. gogo, Adenanthera gogo, E. pursaetha and E. monostachya. Doubtless both lianas were used in a similar manner wherever they were found, although the African literature under Entada phaseoloides certainly refers to E. rheedei, which gained a reputation for being able to intensify dreams. This was the basis of the African Dream Bean’s use by medicine men to commune with the spirits and accounts for more recent interest in its visionary properties. When used for this purpose the seed starch was taken directly or prepared (chopped, dried, mixed with herbs such as tobacco) for use as a smoking agent before sleep (www.entheology.org). However, one does wonder about the chances of experiencing the emetic and purgative attributes of unprocessed or inadequately detoxified seeds. There were very good reasons for the lengthy preparation strategies that accompanied their use. Their bitter, acrid properties have been repeatedly mentioned in the literature. The seeds not only contain saponins, but also alkaloids and oil (6–10%5) components: ‘The oil is said to be poisonous, an idea which may have arisen from its repulsive odour. The process of roasting is said to result in the appearance of a bitter constituent and the disappearance of the repulsive-smelling oil’ (Watt & Breyer-Brandwijk 1962). Entada seeds have been deliberately employed as an emetic in India, while the root infusion was used for similar purposes in Africa. The beans have even been utilised as a coffee substitute in West Africa, although sometimes the purgative action could give a more stimulating effect than was desirable. Javanese women employed the roasted seeds of Entada phaseoloides as a ‘purification’ agent – albeit in small doses, combined with other herbal remedies, which one assumes would have modified the emetic and purgative potential (Watt & Breyer-Brandwijk 1962; Burkill 1935). 4 Entada scandens is a synonym of E. phaseoloides, although the name has also been misapplied to E. rheedei in Australia in the older literature. 5 Burkill also mentions the presence of a high amount (18%) of a yellow, tasteless seed oil, which has been utilised as an illuminant in the Sunda Islands (Burkill 1935).
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
A Multipurpose Medicine
Entada phaseoloides pods on vine.
Many species of Entada have been utilised to promote healing, prevent infection, and provide pain relief. The remedies procured from these vines have made use of just about every part of the plant, as the treatment of abdominal disorders illustrates. African medicine prepared a leaf or bark infusion for use as a tonic and stomachic (Oliver-Bever 1986). In Malaysia an ash made from the pods was poulticed on the abdomen for severe internal complaints, while in the Philippines the seed poultice was used for abdominal disorders
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and colic in children (Burkill 1935, Quisumbing 1951). In Indonesian medicine the pounded roots were applied locally, while the stem juice was taken for dysentery and a ‘feverish abdomen’. The roasted seeds could also be taken in small doses to treat stomach-ache – while in Tonga the bark infusion was utilised for the same purpose, as well as for the treatment of a variety of ‘mental ailments’ (Whistler 1992; Perry & Metzger 1981). In India the seed paste was applied locally to relieve pains in the loins and joints, for swollen hands and feet, and to ease inflammatory glandular swellings in the axilla (armpit). It was considered particularly useful when these problems were associated with general debility (Watt & Breyer-Brandwijk 1962). Fijian healers have long used Entada leaves for a multitude of medicinal purposes, some of which are linked to anti-parasitic, analgesic, antispasmodic and antimicrobial actions. They included the treatment of filariasis, elephantiasis, venereal disease and thrush (Cambie 1986). A liquid from the root was taken to treat ulcers, as well as for the relief of ‘spasm of the abdominal muscles’ and headache. The stem fluid was regarded as having anti-rheumatic properties useful for alleviating joint and muscle pain. It was also used to treat painful breathing disorders, while an infusion of the stem was taken for some rather diverse conditions including hernia, fish poisoning and gonorrhoea (Weiner 1985). African traditions have employed the genus similarly. On the Ivory Coast stem bark extracts of E. africana were used against intestinal worms and diarrhoea, while the root extract was taken for respiratory disorders (Mamidou 2005). The popular use of Entada abyssinica (powdered leaves) and E. africana (leaf and bark) as dressings for injuries and sores suggests that these remedies had effective antimicrobial properties. This has been supported experimentally, with leaf extracts of the latter showing antibacterial activity against Bacillus cereus. The Zulu took the ground and cooked root of Entada spicata as a syphilis remedy, while the powdered leaf was applied locally to the affected area. A decoction of Entada abyssinica was employed as an anti-rheumatic in Tanganyika (root-bark) and Rwanda (stem, leaf ) – as well as providing a fever and cough remedy (stem, leaf ) (Magassouba 2007; Cos 2002; Watt & Breyer-Brandwijk 1962).
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An Ophthalmic Irritant
Entada abyssinica. (Courtesy: Marco Schmidt, www. westafricanplants.senckenberg.de)
The Splinter Bean (Entada abyssinica) is one of the species that take the form of a tree (hence the alternative name Tree Entada) that resembles the Acacia, although the broad flat bean-containing pods are typically Entada. This species has toxic attributes that would have made it a rather nasty ‘ordeal poison’.6 One particularly unpleasant practice employed the bark juice or sap introduced under the eyelid, which caused substantial irritation and pain that resulted in conjunctivitis (Watt & Breyer-Bandwijk 1962). The bark juice of Entada phaseoloides (now E. rheedi) was similarly ‘painful and irritating to the eye’. Understandably, great care would normally have been taken not to allow the sap any contact with the delicate eye membrane. It is therefore somewhat unexpected to learn that in central Africa the seed of Entada abyssinica was also used as ophthalmic remedy. Processing would have, doubtless, reduced its irritant potential. The seed was heated to make it ‘pop’ and the contents powdered and made into a weak eye-drop solution. A cold infusion of Entada africana root has been similarly utilised as a lotion for sore eyes (Watt & Breyer-Brandwijk 1962). 6 ‘Ordeal poisons’ are poisons used for a specific purpose involving the administration of tribal justice.
The genus has been recommended for respiratory disorders and fevers in a number of other countries. In Burma, Matchbox Bean seeds were used as a febrifuge (Perry & Metzger 1981). In the Amazon the seed decoction of Entada polyphylla was employed as a gargle for cases of serious catarrhal congestion of the respiratory tract and sinuses (Schultes & Raffauf 1990). In Angola and the Belgian Congo, a bark decoction of Entada abyssinica was likewise recommended for chronic bronchial congestion and as a febrifuge. In Africa, a strong decoction of Entada spicata root has been employed for treating sharp chest pains that were non-tubercular in origin. The bark has even been given to horses as a cold remedy (Watt & Breyer-Brandwijk 1962). Some of these claims may be verifiable. Recent investigations of Entada africana, which has been used in Mali for treating fevers and a range of respiratory problems, demonstrated potent bronchodilatory and antitussive activity (Occhiuto 1999).
Daintree River tour guide David Sperling with pods of the Matchbox Bean (Entada phaseoloides). Matchbox Bean flowers on right.
The Matchbox Bean has been recommended for gynaecological problems in a number of different cultures. It was deployed as a contraceptive, in combination with Dioscorea bulbifera, by Aboriginal people at Cape York. While the chemical basis of the claim remains unknown it could possibly be related to toxic seed components. Early in the morning the seed was eaten (raw or roasted) on an empty stomach. The
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
woman then rested and did not drink throughout the day. Although it was thought to produce temporary sterility, mention has been made that the effect could be permanent (Watt & Breyer-Brandwick 1962; Webb 1959). A similar use of Entada purseatha in India has been reported – the seed prepared as tablets with jaggery (unrefined whole cane sugar). The remedy was given after menstruation for a period of five days to ‘induce permanent sterility’ (Vijayakumar & Pullaiah 1998). In Fijian herbal medicine the leaves were used in a multitude of ways during parturition. This included treatments to shorten the period of labour, as well as to assist removal of the afterbirth, and as a tonic for weakness after the birth (Cambie 1986). In Africa, Entada africana was reported to have abortifacient effects, while E. phaseoloides seeds provided a remedy for ‘difficult parturition’. In Tanganyika Entada abyssinica was also used in the treatment of miscarriage (Watt & Breyer-Brandwijk 1962). Most of these remedies suggest a hormonal influence, which would appear to be quite significant.
The traditional medicinal use of the Entada genus has prompted more detailed investigations which have indicated that these plants have interesting antiparasitic, anti-microbial and antiinflammatory potential. In addition to saponins, there are diverse components of pharmacological interest in the genus. The chemical composition of E. africana, E. abyssinica and E. phaseoloides appears to be very similar. Stem bark extracts of Entada africana (which is a shrub or small tree) were shown to be strongly positive for alkaloids, cardiac glycosides, terpenoids, steroids, anthraquinones and tannins. Flavonoids and amino acids were also present. This species has been widely used for treating fevers (including malaria), infectious disorders (coughs, colds, tuberculosis), Herpes infections, diabetes, candidiasis, gonorrhoea, diarrhoea and hepatitis. Root and leaf extracts, which can have a high phenolic content, have shown strong antioxidant properties that support its therapeutic reputation. Other studies have
Validating Traditional Remedies
Entada africana. (Courtesy: Annette Gockele, www. westafricanplants.senckenberg.de)
The saponin-containing Entada genus has been widely used for fish-poisoning purposes. Indeed, the tropical African species Entada africana, which contains saponins and rotenone, has shown piscicidal properties at a dilution of 1:1000 (Oliver-Bever 1986). (Image courtesy: Marco Schmidt, www.westafricanplants. senckenberg.de)
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shown blood sugar lowering (hypoglycaemic) and hepatoprotective potential. Stem bark extracts have demonstrated antibacterial activity against Salmonella typhi. In Ghana two other herbs, Mimosa pigra and Acacia nilotica (which were traditionally combined with E. africana), were similarly active against S. typhi. These findings support the use of the combined remedy against typhoid fever (Mbatchou 2011; Tibri 2010 & 2007; Njayou 2008; Kisangau 2007). Nigerian investigations have revealed interesting antimicrobial activity against the causative organism for cholera (Vibrio cholerae) (Akinsinde & Olukoya 1996). There are other studies that indicate some less familiar species possess similar antibacterial properties. Kenyan investigations of Entada leptostachya (root extracts) showed or demonstrated fair to good antibacterial activity against Escherichia coli, Bacillus subtilis and Staphylococcus aureus. This species has been used as an anthelmintic, and sap from the crushed stem was applied locally as an antidote for snake bite (Kareru 2008). Malaysian studies of Entada spiralis stem bark have shown antifungal activity against dermatophytes responsible for skin disorders including tinea (Harun 2011; Owur & Kisangau 2006). Studies of Entada abyssinica (leaf extracts) have established antifungal and antibacterial attributes – as well as anti-inflammatory activity that could possibly be linked to the presence of flavonoids. In addition, the presence of polysaccharides in root extracts tends to support the use of this species as a wound healing agent (Diallo 2001; Olajide & Alada 2001; Fabry 1998 & 1996a). Leaf extracts were shown to be highly active against the mosquito-borne Semliki Forest virus, as well as having moderate activity against Coxsackie and Polio viruses (Cos 2002). Entada phaseoloides also contains unique anti-inflammatory compounds (entadamide A and B) (Ikegami 1989). Certainly, the chemical basis underlying many folk uses of the genus have only begun to be examined, with some research findings suggesting greater therapeutic potential. For instance, the use
of Entada phaseoloides as a tonic against cancer in Fiji has gained support from a number of studies. One of the seed saponins (prosapogenin) has exhibited anti-tumour properties (Dai 1991; Cambie 1986). Studies of African samples of Entada africana and E. rheedii isolated triterpene saponins (e.g. rheediinosides) with antioxidant and anticancer (antiproliferative and cytotoxic) potential (Nzowa 2010; Cioffi 2006). The Entada genus contains a number of candidates with antiparasitic activity. Early studies determined that Entada saponins were strongly haemolytic, with reports of an anti-amoebic effect against the parasite responsible for dysentery. Blood cells and amoebae were: ‘destroyed by the saponin, the cells bursting with explosive violence’ (Watt & Breyer-Brandwijk 1962). More recent investigations provide additional support for their traditional deployment: • Entada africana showed good activity against the Leishmania parasite (Ahua 2007). • Entada abyssinica has been used in Uganda for the treatment of sleeping sickness, a parasiteinduced condition due to Trypanosoma. Experiments isolated a diterpene identified as kolavenol7 with activity against Trypanosoma brucei rhodesiense, which is one of the two causative agents of sleeping sickness (Nyasse 2004; Freiburghaus 1998 & 1996). • Matchbox Bean (Entada phaseoloides) extracts had molluscicidal properties against the snail host for Schistosoma japonicum. Unfortunately, although the plant extract was very stable in a wide range of conditions, field trials revealed that the effective concentration of the bark was too high (40 g/m2) for practical use (Yasuraoka 1977). The tannin-containing bark of Entada africana has also demonstrated molluscicidal activity (Ayoub Hussein & Yakov 1986). 7 Kolavenol has been found in a couple of botanically unrelated plants such as the resin-yielding genus Copaifera (C. officinalis, C. langsdorffii, C. reticulata), where it attracted serious investigation as an anticancer agent (Ohsaki 1994). The related diterpene, kaurenoic acid, which has shown good antimicrobial and anti-inflammatory properties, was found to be equally interesting due to its anticancer activity against breast and colon cancer cells, as well as having anti-leukaemic attributes (Paiva 2002; Costa-Lotufo 2002).
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
Wild Food: Foraging for Yams
Native plant tubers are an obvious food choice although the large number of species that can be utilised may come as a surprise. While yams were a popular staple dietary item in the northern regions of Australia, in more temperate regions other resources were utilised. Few would have been as plentiful, or as valued, however, as those harvested from the Dioscorea genus, which were primarily available throughout the tropical regions of the continent. The processing that was essential to achieving culinary acceptability was similar to that undertaken in Asia and the Pacific. Even in the earliest days of European exploration in Australia, the dietary habits of the local inhabitants attracted interest. The Endeavour Journal of Joseph Banks (1768–1771) included the following observations: Of Land animal they probably eat every kind that they can kill which probably does not amount to any large number, every species being here shy and cautious in a high degree. The only vegetables we saw them use were Yams of 2 sorts, the one long and like a finger, the other round and covered with stringy roots, both sort very small but sweet; they were so scarce where we were that we never could find the plants that produced them, tho we often saw the places where they had been dug up by the Indians very newly. It is very probable that the Dry season which was at its height when we were there had destroyed the leaves of the plants so that we had no guides, while the Indians knowing well the stalks might find them easily (Beaglehole 1963).
These descriptions appear to refer to the Long Yam, Dioscorea transversa, and the Round Yam, Dioscorea bulbifera. As Banks surmised, the foliage of the yam vines dies down during the dry season. This can make them difficult to locate and tracking a withered vine to its source can become a painstaking undertaking. Accurate species selection and canny foraging skills were essential for a good harvest. A familiarity with the traditional collection sites of the tuber made the search easier – and those with forethought would replant a piece of the root to ensure future crops. Sometimes the search could develop into a difficult venture, even prohibitively so, if the tubers rooted deeply into the soil. At times the tuber was simply too well buried to be worth the effort of extraction.
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Native Grapes and Tubers
Ampellocissus acetosa. (Detail image flowering vine courtesy: Tony Rodd,
‘Native Grapes’ belong to the Vitaceae – the same family as wine-producing grape vines, although the fruit is not equally palatable. Ampellocissus acetosa and A. frutescens yield attractive dark purple globular grape-like fruits that, while edible, are not favoured due to their strong, unpleasant aftertaste. They, and various other species such as Cissus adnata, have ‘cheeky’ (irritant) properties that can result in a burning sensation in the throat. A few of these vines also yield an edible taproot, albeit not a particularly sought-after vegetable as
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it can retain irritant qualities, even after substantial preparation. In the Northern Territory the juice from these Native Grapes (Ampellocissus acetosa and A. frutescens) was used as an antidote for snake bite, including that of the Death Adder, Acanthophis antarcticus (Hiddins 2001).
Cayratia trifolia.
The Bitter Potato was sourced from a related Vitaceae species, Cayratia trifolia. This was available during winter (April–August) when tuber growth was at its best. Preparation involves mashing the root between rocks before it is roasted in ashes (Smith 1993; Wightman 1991). This yam also held an interesting ritual and spiritual connections with the wet season in the Northern Territory. The root, mashed up and mixed with some mud, was ceremonially fashioned into cloudy shapes – a rite that was designed to encourage the seasonal rains to begin (Lindsay 2001; Marrfurra 1995). Vigna tubers can be equally useful food resources. That of the Long Yam (Vigna lanceolata) can be eaten raw or after roasting in campfire ashes, although sometimes extremely fibrous tubers required crushing before use. The tastiest yams are harvested at the beginning of the dry season, following the end of the monsoonal rains. While Vigna vexillata has a similar pleasant flavour, the flesh is habitually fibrous. This species was harvested during the middle of the dry season in the Northern Territory (Lindsay 2001; Marrfurra 1995; Wightman 1994). The lovely Fringed Lilies (genus Thysanotus), which are found throughout the continent, produce small roots that swell to form small
Seeds of Vigna radiata (square length 5 mm). A number of wild Vigna yield edible seeds that have been compared to peas or mung beans, e.g. V. radiata, V. vexillata, V. lanceolata (var. lanceolata and var. filiformis). (Image courtesy: Sarefo, Wikimedia Commons)
edible sugary tubers. In the past species such as Thysanotus tuberosus and T. patersonii were harvested, although many others are likely to have been regarded as equally useful local forage. The latter is widespread across the southern half of the continent (including Tasmania). In Western Australia the fire-cooked vine was powdered and eaten as a condiment with the root of the York Gum (Eucalyptus loxophleba) (Low 1992b). In the Northern Territory the tuber of a tropical coastal species, Thysanotus banksii, was harvested after the rainy season, sometimes in large quantities, when the flooded creeks and rivers begin to recede to normal levels. These small tubers possess a nutty flavour and are very tasty both raw and lightly roasted (Lindsay 2001). The tubers of the Desert Fringed Lily (Thysanotus exiliflorus) have also provided a welcome water resource throughout the arid regions of the country (Central Australia, Western Australia, South Australia) (Low 1992b). Thysanotus tuberosus. (Courtesy: KAW Williams, Native Plants of Queensland, Vol. 3)
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Riverine resources include water plants such as the Spike Rush (genus Eleocharis) and Bulrush (Typha domingensis, T. latifolia, T. orientalis) that often produce small tubers that are useful food resources. Eleocharis nuda is a Spike Rush of the Northern Territory and Queensland, while E. acuta is widespread throughout the southern states. (Image E. acuta on right, courtesy: KAW Williams, Native Plants of Queensland, Vol. 3; image E. nuda on left, courtesy: KAW Williams, Native Plants of Queensland, Vol. 2)
Food resources are usually subject to seasonal availability. Distinct clues, such as when leaves turn yellow and die, or when grass seeds burst, indicate harvesting times. Food-gathering practices that followed the seasons were considered to be in harmony with the spirits of the land – a philosophy integral to the Aboriginal lifestyle. Many tribes regarded the harvesting of root vegetables and fruits as ‘women’s work’ – recognising this as an important task that required a considerable amount of skill. Choices included the tuberous stems of a number of species normally found in billabongs and lakes: Cyperus macrostachyos and C. bulbosus, the Bulrush (Typha domingensis) and the Water Ribbon Yam (Triglochin dubium) (Lindsay 2001; Yunupinu 1995; Smith 1993, Smith & Wightman 1990). Tubers of the Water Chestnut (Eleocharis sphacelata, E. dulcis), which were found at waterhole edges, were usually roasted and peeled before use – although some types could be eaten raw (Lindsay 2001; Marrfurra 1995; Wightman 1994 & 1992). Another useful resource is the Water Yam (Aponogeton vanbruggenii), a riverine species that yields small tubers that are a useful source of water, particularly in dry spells. In addition, the flowers were once employed as a filling for small pillows (Lindsay 2001). Studies have shown that many of these traditional foods have serious benefits as low GI (glycaemic index) foods8, which means that the starch they contain is released slowly in comparison to that in many Western products, such as white flour goods (breads, cakes),
Cooked and mashed, the corms of the Water Ribbon or Creek Lily (Triglochin procera) are suitable for young children (5–6 months old) (Levitt 1981). (Image courtesy: Colleen Miller)
pasta (white spaghetti), potatoes and white rice, which all have a fast-release (high GI) pattern. Those of interest include species of Vigna including the Pencil Yam (Vigna lanceolata), Native Potatoes from the Ipomoea genus (notably I. polpha and I. costata), native Dioscorea yams such as the Long Yam (D. transversa) and Cheeky Yam (D. bulbifera), the Native Arrowroot (Tacca leontopetaloides), Bush Onion (Cyperus bulbosus), Pigweed (Portulaca oleracea), Saltbush (Trianthema triquentra) and a few native ‘lilies’, among them the Vanilla Lily (Arthropodium milleflorum), Blue Grass Lily (Caesia vittata) and Flax Lily (Dianella laevis) (Thorburn 1987). There are many more candidates. The low GI index of many traditional foods is fortunate because Aboriginal people have a high risk of developing diabetes – genetically they are hardwired for a hunter-gatherer lifestyle, not a starchy European-style diet. However, most of us today, regardless of genetic heritage, also run a much higher risk of diabetes than was the case even up to the mid twentieth century. This is due to the consumption of modern fast foods and highly refined and processed items. Some years ago Anne Thorburn recommended: 8 The GI level of foods is often independent of the fibre content. Low and high fibre foods may have similar glycaemic activity (Thorburn 1987).
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‘A greater understanding of which aspects of modern western lifestyle act to trigger disease may suggest new approaches to its prevention and treatment. Slowrelease carbohydrates in traditional diets need to be explored as one of a number of factors that, in varying degrees of magnitude, play a role in preventing the expression of diabetes. In the meantime our findings suggest that slow-release, low-fat, traditional staples can be recommended as part of the dietary treatment of diabetes for Australian Aborigines and Pacific Islanders’ (Thorburn 1987). Indeed, all diabetics would find these strategies beneficial. However, the risk of diabetic complications such as kidney failure and retinopathy is particularly high for Aboriginal people. There is also a substantially increased risk of cardiovascular disease – conditions that are seriously compromised by poor dietary habits. Certainly there is a lot of support for the cultivation and consumption of bush foods, particularly in remote regions of Australia where it is often difficult to source fresh fruit and vegetables.
Golden-flowered Medicinals
The Grass Yam, Curculigo ensifolia, is a tropical lily-like Australian herb with a long, narrow type of yam which was lightly roasted before being eaten (Lindsay 2001). Interestingly, some plants in the genus contain a sweetener and taste-modifying protein (neoculin) that can convert a sour flavour into sweetness (Nakajima 2011; Okubo 2008). The mucilage from the rhizome has also attracted interest as a suspension agent for pharmaceutical use, with qualities that were equivalent (or superior) to Acacia Gum (Gaikar 2011).
Curculigo orchioides, from Plants of the Coast of Coromandel, W Roxburgh (1793).
The Grass Yam (Curculigo ensifolia) is a native species about which little is known as a medicinal herb – although a close relative, Curculigo orchioides (Black Musli), has been a respected remedy in Ayurvedic and Chinese medicine. In
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
India, the mucilage-rich rhizome is regarded as being a bitter aromatic tonic, with demulcent, diuretic and aphrodisiac properties, and was often administered with sugar and/or milk. The herb has numerous uses: for treating age-related debility, chronic fatigue, respiratory distress (asthma, bronchitis), genitourinary problems (gonorrhoea, leucorrhoea, to remove urinary tract stones), digestive tract problems (biliousness, haemorrhoids, diarrhoea, worm infestation), jaundice, low back pain (lumbago) – and has even been utilised for treating eye disorders (ophthalmia). The rhizome paste has also been applied locally as a poultice for itching skin problems, or the plant juice for cuts and wounds (Kapoor 1990; Chopra 1956). Investigations have recently provided support for many of these recommendations, confirming antioxdiant, anti-inflammatory, wound healing, hepatoprotective, antidiabetic and potential anticancer activity (Chauhan 2010; Agrahari 2010a & 2010b; Yokosuka 2010; Venukurar & Latha 2002). Rhizome extracts (steam distilled) have shown exceptionally high antibacterial activity against Staphylococcus aureus and a good level of activity against S. epidermis. This suggests that the essential oil would be a useful antiseptic agent (Nagesh & Shanthamma 2009). Other studies have shown root extracts were active against Pseudomonas aeruginosa, Bacillus subtilis and Escherichia coli. Antifungal activity was not seen in one study, although antiCandida properties were demonstrated in another
(Menghani 2011; Jagtap 2010). Black Musli has substantial antispasmodic, immune stimulant and anti-histaminic properties that are of interest for treating allergy, immune suppression and asthma (Rathod 2010; Venkatesh 2009; Pandit 2008; Bafna & Mishra 2006; Lakshmi 2003). Phenolic glycosides, which are also found in Curculigo crassifolia, have been of particular interest as the active antioxidant components of rhizome extracts – as well as having anti-osteoporotic potential (Jiao 2009; Wang 2007; Wu 2005). In particular, curculigoside (a major phenolic in extracts)9 has undergone serious investigation as it appears to be linked to the ability of the herb to promote bone and fracture healing. The remedy has experimental anti-osteoporosis properties that could be of serious interest to individuals suffering from a loss of bone integrity, particularly post-menopausal women. These findings support the traditional use of the rhizome in Chinese medicine as a tonic for back and knee weakness and joint problems (arthritis). The effect may be linked, at least in part, to an oestrogenic activity (Ma 2011; Jiao 2009; Lee 2009; Cao 2008; Kapoor 2008; Vijayanarayana 2007; Wong 2007). However, the herb has also shown tonic, adaptogen and androgen-like effects with male aphrodisiac and fertility-enhancing properties – which have been supported by a number of studies (Thakur 2011 & 2009; Chauhan & Dixit 2008; Chauhan 2007; Chen 1989). In addition there are some very interesting studies showing antioxidant, neuroprotective, anticonvulsant and sedative effects with potential for use as a protective agent against ischaemia (loss of blood supply) in brain injury or cardiovascular distress, as well as damage leading to hearing loss. Curculigoside continues to be a major compound of pharmaceutical interest (Hong 2011; Wang 2010; Chen 1989). In addition the herb has potential for minimising drug side-effects and modification of the anorexia and nausea associated with chemotherapy medications (Kapoor 2008; Saxena 2008).
Black Musli or Yellow Ground Star, Curculigo orchioides. (Courtesy: Viren Vaz – CC by SA2.5)
9 While there are a number of phenolics that have shown antiosteoporotic activity from this herb, curculigoside has been the main subject of research (see Jiang 2009 for further details).
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The Yam Daisy: A Native Snack Food (Microseris lanceolata)
The Yam Daisy or Murnong (Microseris lanceolata) is found in New South Wales, Tasmania and Victoria. Although this species is listed as having a number of synonyms (including M. scapigera) there may actually be a couple of different species in the genus which have not, as yet, been botanically defined. (Image courtesy: Knox Environment Society)
is one of the native herbs that has been a casualty of European colonisation. The plant was once widely found throughout South Australia and in some parts of New South Wales, but the introduction of cattle and sheep, which found it particularly palatable, ensured its eradication from much of its natural habitat. Murnong is an interesting Australian member of the Asteraceae family that, despite its name, is not related to the common Yams from the genera Dioscorea (family Dioscoreaceae) or Ipomoea (family Convolvulaceae). Yam Daisy is placed in the tribe Lactuceae, with other leafy edible greens such as Lettuce, Chicory, Dandelion, Salsify and Sow Thistle. This accounts for its resemblance to Dandelion (Taraxacum officinale) and Common Catsear (Hypocheris radicata). Murnong tubers can be eaten either raw or roasted. Joseph Maiden (1900b) noted the following under Microseris Forsteri: ‘The tubers were largely used as food by the aborigines. They are sweet and milky, and in flavour resemble the cocoanut. Mr. Brough Smyth (Aboriginals of Victoria, i, 209) describes them as small, in taste rather sweet, not unpleasant and perhaps more like a radish than
a potato. Baron von Mueller has suggested their cultivation with the view to their improvement as a vegetable.’ Murnong root is of dietary interest as it is a carbohydrate-rich resource that contains a large amount of inulin, a polysaccharide that is utilised by the plant as a food reserve. Murnong also contains small amounts of protein, fats, carotenoids and fatty acids. Inulin-containing vegetables (asparagus, leek, onion, artichoke, chicory root) have been recommended in specialised diets, particularly for diabetics. Their metabolic benefits involve the regulation of carbohydrate and lipid metabolism with a resultant lowering of blood glucose levels and improvement in insulin sensitivity – as well as reductions in blood urea and uric acid levels. Inulin is found in a number of other Asteraceae – notably Elecampane (Inula helenium), the Jerusalem Artichoke (Helianthus tuberosus) and Chicory (Cichorium intybus). The latter two are the main sources of inulin and oligofructose for the commercial food industry. They are used in cheeses, yoghurt, baked goods, chocolate, ice cream, sauces, dairy-based desserts, confectionery and fruit preparations. These compounds, which are fairly tasteless, have been attributed with probiotic effects – albeit they are not directly utilised by the human intestine. They appear to work by stimulating the growth of beneficial bifidobacteria, thereby reducing bacterial fermentation in the gut. Their incorporation into the diet might help to assuage hunger without contributing any undesirable calories – as well as being supportive to colonic function and alleviating constipation. Other beneficial attributes of these polysaccharides involve stimulation of the immune system, promotion of mineral absorption (particularly calcium), and a reduced synthesis of triglycerides and fatty acids in the liver, thereby helping in the treatment of some serious conditions. These include osteoporosis (by raising calcium levels) and atherosclerosis (by reducing cholesterol levels), and a lowered incidence of colon cancer has been reported (Kaur & Gupta 2002).
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Dioscorea: Yams of Distinction
Microseris lanceolata (syn. M. scapigera) contains reasonable amounts (mg/100 g) of fibre (7–11 mg) and carbohydrate (10–21 mg), low protein and fat levels, and can be a useful water resource (73–79 mg). In addition it contains a good range of minerals: potassium (156–251 mg), sodium (18–27 mg), magnesium (18–34 mg) and calcium (19–27 mg). The iron levels can be quite high (1.7–7.8 mg) – with very small amounts of zinc (0.3–1 mg) and copper (0.1–0.4 mg) (Brand Miller 1993). (Image courtesy: S Aubertuniv Grenoble, SAJF [Station Alpine Joseph Fourier])
Leaves of Dioscorea transversa. (Courtesy: FloraNQ, flckr)
Jerusalem Artichoke (Helianthus tuberosus) tubers, which are actually subterranean stems, have a reputation similar to that of the potato. They contain 11–26% sucrose, a high proportion of inulin (31– 60%) and 27–40% levulin (synanthrin, an inulin isomer). The tuber can be used to produce a highfructose syrup (70–80% fructose, 20–30% glucose) that has been a particularly useful sweetener for culinary items such as bakery products or various processed foods. The stem and root have also shown antibiotic activity (Watt & Breyer-Brandwijk 1962). (Image courtesy: Gila Brand, Wikipedia)
Dioscorea transversa (fruiting vine). (Courtesy: KAW Williams, Native Plants of Queensland, Vol. 1)
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The early explorers, who were avid observers of the use and availability of local food resources (their lives could depend on it), mentioned procuring yams in the outback regions of Australia. The Round Yam (Dioscorea bulbifera) and the Long Yam (D. transversa) were among those regarded as being particularly useful vegetables in the subtropical and tropical regions. During his travels in northern Queensland in 1883, Edward Palmer described Dioscorea transversa: ‘a yam of large size, something like a sweet potato … The vine climbs to the tops of trees in the scrub, the seeds gathering in large clusters; thin light seeds, like brown paper. The roots grow among rocks in the crevices where rich soil is to be found. Mostly eaten raw, larger ones roasted.’ In general, yams are not very palatable raw and require cooking. Indeed, the tubers of most species require thorough detoxification to remove compounds that either taste quite awful or have irritant properties. Unfortunately, some species harbour both disadvantages. Yams have been utilised as vegetables throughout much of tropical Australia and Asia, due to their local availability, but their palatability can vary substantially. This is because the majority of the world’s 600 Dioscorea yam species have a bitter characteristic. Overall, only a dozen or so are suited for culinary use. In addition, their appeal as a vegetable is compromised by the fact that they do not tend to cook as easily as the cultivated potato from South America. Henry Burkill (1935) made the following observations in this regard: The tubers [of Dioscorea alata] are starchy10, but not so completely as a potato. When boiled, they retain a considerable measure of stickiness, which renders them somewhat indigestible. They need steaming for the table, and a cook able to prepare potatoes well, may not be expert enough to prepare yams equally well. That circumstance, alone, is sufficient to explain why the potato, with the aid of transport is ousting the yam from its markets. Manihot has also taken part in displacing yams, because its cultivation is so easy. In rice-countries, their hold has never been as strong as in others; thus, as [Georg Eberhard] Rumpf explained, yams were used by inclination in Java, while they were used of necessity in Celebes [Sulawesi] and Boeton [Indonesia].
10 Total starch content ranges around 7.8–10.27%. Cooking (steaming) results in a significant increase in the total starch content, although long-term storage can substantially decrease this, by 20–30% (Ahmed & Urooj 2008).
In addition, a few yam species are utilised medicinally, although these are not suited for the table as they usually possess a heightened bitter characteristic due to their chemical components. Agricultural practices tend to reduce the toxic potential of cultivated crops. The poisonous qualities are gradually removed by selective breeding, which also tends to place an emphasis on larger, more palatable varieties (Denham 2007). Henry Burkill (1935) provides a wonderful explanation of reasons behind the natural evolutionary process associated with yam development: They [Dioscorea yams] have underground storage organs that enable the plant to renew annually a vigorous growth and to rest through less favourable months. These storage organs, if thrust deep into the ground, are sufficiently protected against wild hogs and other animals by soil above them, but there are many species which lie superficially in the soil and escape destruction because they are protected by poisonous substances in their flesh or, in a few species, by a covering of thorny roots. Man, when it is worth his while, digs up the storage organs of deep-rooting species to use as food: in regard to others he has discovered means of destroying, or removing the poisons and, doing that, eats their storage organs likewise. By cultivation he has selected superficially rooting races, and even evolved species out of those that root deeply, substituting his own methods of protecting his crop for the natural protection of deep-rooting; and he has greatly reduced poisonousness of certain selected varieties derived from the other group. Among those species which he has appropriated for cultivation, the Asiatic Dioscorea alata, Linn., is the most used, and has been so modified that it is barely able to persist without the protection of man. The African D. rotundata, Poir., and D. cayenensis, Lam., demand approximately an equivalent amount of protection. The tropical Asiatic D. esculenta, Burkill, may be regarded as the fourth yam in order of importance to man; the Chinese D. opposita, Thunb.11, and the American D. trifida, Linn., as the fifth and sixth.
Burkill rated Dioscorea bulbifera, D. pentaphylla, D. dumetorum and D. hispida of far less value, although ‘to the most primitive of man – the food-gatherers – almost every wild species of the Old World has some importance’. 11 Duke & Ayensu (1985) mention that Dioscorea opposita and D. japonica are temperate species native to China and Japan that have sometimes been classified under the invalid name D. batatas. In this section the latter name is used as per the reference that is cited.
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Identification Matters
Dioscorea pentaphylla vine. (Courtesy: Kim and Forest Starr, Hawaii) Dioscorea alata flowering vine. (Courtesy: Kim and Forest Starr, Hawaii)
Five Dioscorea species are found in the northern Australian tropics, with an additional species favouring a southern temperate climate. Because the leaf shape often resembles that of many other jungle vines, identification can be difficult with the individual species hard to distinguish unless one is familiar with the variations in venation. The minute flowers form strings of blossoms, which are not easily seen and later give way to more noticeable clusters of flat seed pods – although they all too quickly float away into the forest canopy to be of much use for identification purposes. These vines are generally characterised by attractive heart-shaped leaves with veins radiating from the stalk attachment point. The Round Yam (Dioscorea bulbifera) and the Long Yam (D. transversa) are quite common in the northern tropics. Although these vines have a similar appearance, the leaves of the latter are smaller. The Warrine or Warrien (Dioscorea hastifolia) is a Western Australian species of the open forest that is found in the southern part of the state. In addition, there is the highly valued Greater Yam (Dioscorea alata), a luxuriant leafy vine that yields a very large tuber. The Five-leaf Yam (Dioscorea pentaphylla) of Thursday and Hammond Islands has distinctive five-lobed leaves and appears to have been cultivated there from ancient times (Low 1992a).
Overall Dioscorea tubers have been found a reasonable carbohydrate and dietary fibre resource. Generally the level of sodium was low and small amounts of zinc were present, with variable amounts of a few other minerals of interest in the different species (Brand-Miller 1993): • Dioscorea alata: some calcium; moderate potassium (150–430 mg/100 g); low magnesium (9–21 mg); moderate iron (0.7–1.1 mg). • Dioscorea bulbifera: potassium could be high (70–597 mg); magnesium (13–24 mg); variable calcium (2–65 mg); iron ranged from low to high (0.7–12.3 mg). • Dioscorea transversa: some samples contained sodium (50 mg), potassium 180–380 mg (one sample was higher: 1142 mg); magnesium (17– 224 mg), variable calcium (3–230 mg); iron (1.8–14.1 mg).
In many parts of the world the Yam was so intensively cultivated that certain varieties came to dominate the crop. These were chosen for their palatability, gradually displacing those with undue bitterness. The toxic wild races were phased out over time, resulting in the selective cultivation of less poisonous varieties. Eventually, some species evolved into viable food crops, with toxicity generally limited to the upper part of the tuber – although wild species still exist with poisonous potential (Burkill 1935).
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Henry Burkill explains further: There is a substance in the raw tubers, even in those which seem to be among the most innocuous, with an irritant action. It makes the skin of the fingers to tingle slightly by continued contact; on the throat and tongue the irritation due to it is distinctly unpleasant. Even D .alata when raw produces this effect and in quantity causes stupefaction. It is uncertain what the substance is. It is probable that to its action is due the use of yam roots in India as a poultice to reduce swellings, and perhaps, also, their use upon snake and scorpion bites. Malays make similar application to the sores of syphilis and leprosy (Burkill 1935).
The Greater Yam (Dioscorea alata) has been so long in cultivation that the original wild sources of the plant remain a mystery. Over time it has become widely distributed throughout Asia and the Pacific – and there are a number of populations in northern Australia, the origins of which have engendered considerable debate. Certainly the presence of the plant in Arnhem Land and on the north-east Queensland coast could not have occurred without deliberate human intervention. The tuber may well have arrived with Macassan traders, who came fishing for bêche-de-mer in the region around the early 1700s. However, not all wild plant sites fit with this explanation. The fact that widely different locations are involved provides some support for the idea that the yam was brought to this country long before – possibly when the Australian landmass was still linked to New Guinea (over 8000 years ago) where Dioscorea alata has a long history of cultivation as a staple food crop (Denham 1993). Edward Palmer’s description of the Greater Yam provides another good illustration of how lengthy processing can be. He described the vine as: very abundant in the wet season. Large heart-shaped leaf and small pendant flowers. Has numerous large tubers with hairy roots from all sides, very bitter. They are gathered and stored in sand about their [the Aborigines’] old camps. When using them the tubers are first roasted, then broken in water and strained through fine bags into large bark troughs full of water, and washed for hours, running the water over the sides of the plant troughs as it gets discoloured, and stirring the yellow fecula [a starchy substance with thickening qualities] with the hands. When sufficiently washed, round basins are made in the sand and lined with soft clay and sand, into which the product is poured; when much of the intermixed water
held is drained away, leaving the food fit for use, and looking very much like maize hominy. Leichhardt speaks of finding these tubers in the blacks’ camps … and finding difficulty in using them owing to their intense bitterness (Palmer 1883).
A number of components are responsible for the toxic qualities of the various yams, although many of the irritant compounds are water-soluble and can usually be removed (or detoxified) during the cooking process. Certainly some of the discomforting symptoms appear to be due to the irritant effects of oxalates (oxalic acid), although the tubers may also contain histamine (an allergen). Other components with anti-nutritional or toxic potential include phenols, tannins and hydrogen cyanide (HCN). Oxalates and HCN can have a direct toxic effect, while high levels of phenolics (phenols, tannins) can inhibit the activity of digestive enzymes (amylase, trypsin, chymotrypsin, lipase). Fortunately, the compounds that compromise the digestibility of the food via amylase inhibitor activity and trypsin inhibitor activity are usually inactivated during cooking (Shanthakumari 2008). This type of activity is often cited as the ‘anti-nutritional’ component of beans from the Fabaceae family such as broadbeans and soybeans. The intense bitterness that plagues some Dioscorea yams is due to water-soluble diterpenes (e.g. diosbulbins). Studies have found that a bitter characteristic is fairly common, although the potency of the compounds responsible can vary, thereby significantly influencing the yams’ palatability. For instance, evaluations of diosbulbins A and B, which were present in Nepalese wild yams, found that the latter was more potent (Bhandari & Kawabata 2005). However, there are other components with more serious toxic attributes such as steroidal saponins and alkaloids – which are responsible for the exceptionally poisonous reputation of a few species.
A ‘Cheeky’ Yam
The Round Yam (Dioscorea bulbifera), which has also been known as the Hairy Yam due to its distinctive hairy appearance, has an onion-sized tuber with a yellowish flesh. It has been described as a ‘cheeky’ yam, a term referring to its irritant effects when eaten raw, as it causes a burning sensation in the mouth. This
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bulbils and these serve as food. The origin of var. sativa cannot be traced exactly, but the variety seems to have been spread throughout Malaysia and into the Pacific islands long before the arrival of Europeans in the Indian Ocean’ (Burkill 1935). The Australian material was subsequently identified as a different variety altogether: Dioscorea bulbifera var. bulbifera.
Yam Bulbils The Australian Round Yam or Potato Yam (Dioscorea bulbifera, formerly D. sativa) is a common vine of the monsoonal rainforests of northern Queensland.
yam has an international distribution, ranging from Africa, through the Indian subcontinent, to China and tropical Asia. The plant has also emigrated to tropical America and the West Indies. The evolution of this species as a crop was accompanied by a significant measure of varietal selection. Henry Burkill eloquently explains the process: ‘It must have been in past times of greater importance to man as a food plant than it is now. As a result, improved varieties exist which were brought into being at earlier times by his selecting. Selection has been brought into operation not only in the East, but in Africa, with different results, because the original material was varietally different; and the cultivated varieties of Africa can be distinguished readily from those in the East.’ The Australian variety appears to have remained relatively unchanged over time. The three wild varieties of Dioscorea bulbifera found on the Malay Peninsula were the original candidates for its relatives: var. communis, var. heterophylla and var. sativa. The Australian material was originally classified as the latter: ‘In cultivation, and as an escape from cultivation a third, var. sativa, occurs [in Malaysia]. It has larger
Dioscorea bulbifera characteristically produces small aerial yams (bulbils) on its stems late in the wet season. (Courtesy: Kim and Forest Starr, Hawaii)
Dioscorea bulbifera can have a weedy habit due to its large tuberous root and abundant yield of aerial bulbils. The bulbils vary in toxicity depending on their state of maturity and the variety involved. In general, immature or darker coloured bulbils have shown greater toxic potential. Henry Burkill mentioned this variation: ‘The big bulbils of the best races of this variety [var. sativa] are good to eat when properly cooked, and have been
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put to considerable use in certain places. The administrators of the Penal Settlement at Port Blair in the Andaman Islands, about 1880, found the best of its races worth cultivation as a green food for the convicts. The races in the Malay Peninsula are, apparently, not the best.’ It appears that this variability could be substantial, with a somewhat more unusual use of the bulbils in Gabon illustrating their toxic potential. A small portion was added to the local palm wine to promote fermentation. This resulted in a stronger brew with an appealing frothy ‘head’ – but adding too much induced vomiting and severe diarrhoea (Burkill 1985).
Dioscorea sansibarensis. Saponin-containing yams (genus Dioscorea) utilised as fish poisons include D. violacea, D. sansibarensis and the Round Yam (D. bulbifera).
Dioscorea sansibarensis, which bears a resemblance to D. bulbifera, is regarded as being among the less desirable of the African species due to its toxic potential. It has similar large leaves and small airborne tubers (bulbils), albeit the latter are inedible and somewhat bigger than those of D. bulbifera. Floods tend to facilitate its distribution because the bulbils initially sink, resurface later and then float – a very effective natural dispersion strategy. They germinate fairly quickly after the waters recede. In Tanganyika Dioscorea sansibarensis (leaf sap or root decoction) has been used as a remedy for epilepsy (Burkill 1985).
Walter Roth (1901) provided an excellent account of the meticulous processing that attended the use of the native variety of Round Yam (under Dioscorea sativa var. rotunda): On Bloomfield this is suitable for use from about the middle of February to about the middle of May, the approximate extent of the wet season, during which it constitutes the main article of diet … After being dug out, it is carefully washed, and all dirt and adventitious roots removed. It is next baked in a stone oven for about 4 hours, at the end of which time it is mashed up in a grass dilly-bag, and then strained through a dillybag into a bark trough. The dilly-bag remains in the trough, and the yam ‘mash’ to which water has been added, is stirred about and worked up until everything but the fibre and husk strains through into the trough below. The next process is to fill up … the trough with water, to mix the ‘mess’ well up, and allow it to stand therein for a good half-hour or so, i.e. until such time as the water clears, when it is poured off, and fresh water added. It sometimes takes seven or eight waters before the disagreeable taste is removed. As soon as the cook considers it fit, she digs a hole of about the same size and shape as the inside of an ordinary wash-hand basin … in some sandy place … Into this hole the now semi-liquid mass is gently poured, and when the water is all drained off it is ready for eating … looking much like the ordinary preserved (tinned) potato. It has to be eaten the same day as prepared; fermentation takes place quickly … On the Morehead River the preparation is very similar. Rootstocks are cut up into halves or quarters, and washed in a bark trough. Baked in a hot ant-bed covered with tea-tree bark and earth … for about twenty minutes, when it … is transferred into a grass dilly-bag [and] squeezed under water in a trough, the mealy substance passing into the water through the interspaces of the bag … That which has been sieved through sinks to the bottom, the debris etc. rising to the surface of the water, which is then carefully poured off. More water is poured on, the stuff allowed to settle, poured off again, and so on for some four or five times. A circular basin is next hollowed out of the sandy soil, up along the side of which a piece of bark is made to rest … the watery meal is now poured out into the piece of bark, whence it passes gently down into the hole, the water percolating through. As soon as fairly dry it is eaten … the piece of bark resting down the side of the basin-like excavation … is said to prevent the ‘spluttering’ of the meal, which would clog up the interstices of the sand, and so tend to prevent the water passing through.
THE ART OF DETOXIFICATION: REFINING TOXIC PLANTS
Typical earth oven lined with Fan Palm (Licuala) leaves.
The Round Yam has undergone fairly elaborate preparation procedures in various parts of the world. In general, detoxification procedures were similar to those employed in Australia – although in some countries it was regarded as little more than famine food. The tuber was generally peeled, sliced, washed, boiled in lime water (or ash) and soaked for several days. Even so, it was sometimes fed to a dog to ensure its safety. In Malaysia, a type of dough was made from the tubers, which were rasped and kneaded with lime in a coconut shell. The dough was wrapped in a plantain leaf and roasted, or buried and left to ferment. The tubers have also been used as a fish poison, and for washing clothes due to their saponin content (Burkill 1985; Watt & Breyer-Brandwijk 1962; Burkill 1935).
Bush Handicrafts: The Snail Shell Grater Shell from a rainforest snail
large
The ingenious use of local resources can involve a few inventive strategies for making kitchen appliances. On Groote Eylandt in the Northern Territory a snail-shell was fashioned for use as a grater for baked yams. The shell selection was important because soft ones
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broke easily, while the thick shells would not cut cleanly. A hole was poked into the back of the shell (opposite the mouth) to make a simple food grater. The skinned yams were baked until they were soft enough to be easily shredded using the grater, letting the flakes pop through the shell mouth. However, the yams needed to be baked to the right consistency so that they were neither too soft (which clogged up the grater), nor too hard. The yam flesh was collected onto paperbark sheets or into a coolamon and then washed overnight in the creek to remove any residual toxins. A cylinder made from Cycas fronds provided an excellent sieve, the base of which was buried in the sand to prevent it floating away (Levitt 1981).
A Yam of Ancient Origins Dioscorea alata.
The Greater Yam (Dioscorea alata) is an ancient South-east Asian food plant that has been in cultivation for aeons. This vigorous climbing vine can grow up to 15 metres high, producing a large, starch-rich tuber that was greatly valued by travellers.12 Henry Burkill provides details: Early migrations of man carried it out into the Pacific, and medieval voyagers carried it to east Africa; but there is no evidence of its escape from the confines of the Indian and Pacific oceans until in the sixteenth century, the Portuguese carried it round the Cape to their establishments on the Atlantic coasts of Africa and the New World. The keeping properties of the tubers fit them for canoes’ and ships’ stores, and the plant for transport to new countries. The Portuguese slavers seem to have provisioned their ships freely with them, using them to such an extent that there 12 A massive yam, weighing 64 kg and 3.5 m long, has been among the largest tubers grown (Burkill 1985).
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The Greater Yam now has a wide pantropic distribution. The tuber becomes dormant for a couple of months following its growing period, which would have made it easy to carry on long voyages, with the added advantage of being easily propagated upon arrival. The plant is tolerant of poor soil conditions and can be grown where other yams will fail to flourish. The root, however, has the disadvantage of a deep penetrating growth habit that can make it difficult to harvest: The ancestral condition of D. alata was deep-rooting – so deep that man, at a time when he had nothing but a stick to dig with, could not extract the whole tuber. Shallower rooting was desired by him, and selected for, by the care of sporting individuals; yet the deeper rooting plants gave the more tender tubers. Thus it came about that man produced for himself a whole range of races, from such as have tubers descending four and even six feet to such as have tubers which do not descend as much as a foot. He also discovered races in which the response to gravity is abnormal, inasmuch as the tubers curve to a horizontal direction in the soil and even ascend to the surface again. He obtained races with grouped tubers and races with solitary tubers; and he obtained white-fleshed and magenta-fleshed races (Burkill 1935)
Dioscorea alata tuber, from the Philippines. This cultivar has a bright lavender-purple flesh. (Courtesy: Obsidium Soul, Wikimedia Commons project)
Dioscorea alata tuber, cultivar from Hawaii. (Courtesy: Kim and Forest Starr, Hawaii)
Surely, this is a remarkable tribute to the persistence and selective skills of the farmers of the past. Investigations of the genetic heritage of the Greater Yam have confirmed that the centre of variation primarily focuses around Papua New Guinea and Indonesia.13 The vegetable is extremely popular on many Oceanic islands, where substantial diversity can be found. This great range of yam varieties has resulted in a proliferation of tuber shape and colours (from white, cream or yellow hues, to light and dark purple). Shape is an important consideration because tubers that are deformed, flat or triangular tend to be unattractive for marketing purposes, while cylindrical tubers tend to break easily and do not transport well to the markets. Oval or round tubers are more desirable
as they are compact, making them easy to handle and peel before cooking.14 However, shape is not necessarily indicative of edibility, which can be rated quite differently (poor, average and good) depending on amylose/starch ratios. Good-flavoured tubers have a high amylose/starch rating. Some tubers (not all) are also favoured for their sweetness due to their content of natural sugars. In addition, there can be the problem of oxidation of the cut flesh, which can substantially reduce the tubers’ palatability. Oxidation results in colour changes in the flesh, which turns yellowish or brown, and is due to phenolic constituents that also impart off-flavours and bitterness. The reaction can also act as an indicator for special preparation requirements. For propagation purposes, the situation is further complicated by the influence of different chemotypes within a cultivar (Lebot 2005).
13 The varieties of D. alata found in Africa have a more restricted genetic base as they originate from introduced plant clones (Lebot 2005)
14 Dioscorea alata cannot be eaten raw as the uncooked tuber is toxic. Processing involves the normal strategies of peeling, boiling, and baking before use.
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(Satyavati 1976). In north-eastern India a paste made from the tender leaves was employed as an antibacterial remedy for infected skin conditions such as boils (Borthakur & Goswami 1995). Dioscorea alata has been utilised as a tonic in Chinese medicine, which is of interest as studies have shown protective effects on kidney and liver function from toxic chemical damage. The storage protein dioscorin (which should not be confused with the glycoalkaloid dioscorine) present in this species has immunomodulating properties (Lin 2009; Fu 2006; Lee 2002). Storage proteins comprise 1–3% (dry weight basis) of the tuber and are not present in the leaves. While the same type of storage proteins can be found in other yam species, it appears they can differ somewhat in their chemistry and activity. Yam proteins also include phytoglycoproteins (0.2% total dry weight). Those from Dioscorea batatas have shown antioxidant, antiproliferation and antiinflammatory activity. In addition, polysaccharides from the latter have shown immunosupportive activity (Lin 2009; Choi 2004).
• A ‘yam tower’ painstakingly built in celebration of a wedding in Papua New Guinea.
The giant Greater Yam vine fulfils an important customary and religious role in some regions of Papua New Guinea. In the Central Province, yams played an important role in healing practices associated with sorcery – the victim of sorcerous intent was treated with crushed leaves and magical incantations. The yam also gained a medicinal reputation. The leaf, chewed with salt, provided a cough remedy in the New Guinea Highlands. In the Huon Peninsula, Wild Yam root and leaves were used to make a potion that had sedative effects for treating menstrual problems. In addition a decoction of wild yam (root and leaves) was utilised as a sedative for mental disorders: 2–3 cups drunk daily (Holdsworth & Mahana 1983, Holdsworth & Lacanienta 1981, Holdsworth & Giheno 1975). The Greater Yam has an intriguing diversity of medicinal uses. The tuber was regarded as useful for the treatment of leprosy, haemorrhoids and gonorrhoea – as well as being employed as an anthelmintic agent
The search for yam-like tubers in Australia that could be utilised as staple vegetables was to extend beyond the genus Dioscorea. There were a number of interesting native species to choose from, including a few less familiar candidates such as the Spear Lilies from the genus Doryanthes that, although not widespread, were used on a local basis. Plants from the Bindweed family (Convolvulaceae) were found to be quite diverse on this continent and had much in common with those that could be found in Southeast Asia, which suggested they could make a useful harvest. Even so, the tubers of many Impomaea and Convolvulus vines were not particularly palatable and there could be chemical pitfalls associated with their potential use. Some were poor fare due to a stringy or bitter character, or they were simply not substantial enough to be of much value. A few species, however, were certainly worth harvesting – and were a familiar part of the Aboriginal diet, particularly in outback regions. They continue to have an important and interesting future as vegetables, even today.
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Impressive Australian ‘Spear Lilies’
Gymea Lily, Doryanthes excelsa. (Courtesy: PDH, Wikimedia commons project, GFDL, CC-by-SA 2.0)
Artwork by W.H. Fitch, from Gatherings of a Naturalist in Australasia (1860) by G. Bennett. John van Voorst (publisher), Paternoster Row, London.
Australian Spear Lilies were formerly classified as Agavaceae but are now assigned to their own family, Doryanthaceae. The genus name Doryanthes derives from a Greek word meaning ‘spear flower’. They have also been known as Illawarra Lilies or Giant Lilies. There are just two species – the Gymea Lily (Doryanthes excelsa) from New South Wales and D. palmeri from Queensland. These ‘lilies’ produce nectar-rich flowers on spearlike stalks and are a great attraction for wildlife. However, the blossoms are a long-term investment and it can take 10 years before a plant is mature enough to flower. The root and floral stalk of the Gymea Lily have been used for food – although the root required processing and the floral stalk pre-soaking in water before being roasted and eaten. The missionary James Backhouse remarked that the roasted roots were made ‘into a sort of cake, which they eat cold’ (Backhouse 1843). (Left) Doryanthes flowers were a valued nectar resource for Aboriginal people.
Chapter 3
CONVOLVULACEAE: MEDICINAL BUSH FOODS The Convolvulaceae yield a number of edible tuber resources of substantial culinary interest. This family is characterised by twining vines and highly attractive ‘morning glory’ type flowers.1 In particular, the genus Ipomoea contains a good diversity of species in Australia. The most famous root crop from this classification would be the Sweet Potato (Ipomoea batatas) – a viny plant which (like the potato) originated from the Americas. It was transported by Christopher Columbus to Europe. Indeed, this was the ‘potato’ mentioned by Shakespeare – not the Solanum tuberosum crop that is common today. Sweet Potato spread in cultivation throughout Western Europe, Spain and the Mediterranean, later emerging as a staple crop in parts of Southeast Asia. The Chinese, Malays and Indonesians became particularly fond of the vegetable (Burkill 1935). Indeed, China is now the leading country for Sweet Potato cultivation. Worldwide, the production of this crop is around half that of the potato and a quarter that of wheat (Ishida 2000).
Ipomoea indica is a widespread ornamental that can develop a weedy habit.
The genus name is based on the Greek ips or ipos, and homios, terms for ‘worms’ and ‘resemblance’ (i.e. worm-like), which was suggestive of the plants’ twining growth habit. The names ‘morning glory’ or ‘moonflower’, which refer to the times the flowers open, conjure up a much more appealing image. The names Convolvulus (from Latin convolvere, ‘roll together’) and Ipomoea both reflect the fact that many plants in these genera are called ‘bindweeds’ due to their tendency to tangle and twine around other plants. While many native Australian species that were originally classified as Convolvulus were later placed in different classifications (primarily Ipomoea and Merremia), a few species remained as Convolvulus: C. angustissimus, C. clementii,
1 Many species of Convolvulus are known as ‘morning glory’.
Native Bindweeds
The Ipomoea genus is composed of about 500 species that favour the world’s tropics and warm temperate regions. Numerous species are of ornamental value, a few yield tubers suitable for food, while others contain potent chemical compounds, a number of which possess strong purgative properties that have had a recognised place in herbal medicine. ‘Morning glory’ flowers tend to last only for a single day – they open at night and gradually decline as the day progresses. 95
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C. crispifolius, C. erubescens, C. eyreanus, C. gramineus, C. microsepalus, C. recurvatus, C. remotus, C. tedmoorei and C. wimmerensis. Introduced species include Convolvulus arvensis (widespread), C. farinosus (New South Wales) and C. sabatius (Western Australia).
Convolvulus arvensis is an introduced weed that has become naturalised throughout Australia.
Tubers from ‘Morning Glory’ Vines
The Sweet Potato was taken on the epic journeys of settlement across the Pacific Ocean and to New Zealand by the Polynesian people 1500 years ago. Over the centuries it gained such popular acceptance that it is now considered to be the most important staple food throughout the western Pacific region (New Guinea, the Solomon Islands, Irian Jaya). A remarkable achievement for a vegetable that was only introduced into New Guinea around 300 years ago, where it supplanted the use of Taro and, to some extent, the Greater Yam (Dioscorea alata)2, although the latter retained its cultural significance, particularly in the highlands (Bourke 2009). Interestingly, the origins of these crops could vary. New Guinean stocks originated from Indonesia, not the Pacific Islands, while the rootstock that became popular in the Philippines originated from Mexico (Bourke 2009; Burkill 1935). 2 The Lesser Yam or Potato Yam (Dioscorea esculenta), which is equally widely cultivated, was a later introduction and is regarded as having better food value than D. alata (Bourke 2009).
The Sweet Potato appears to have diverse medicinal uses that suggest antibacterial, anti-inflammatory, wound healing and possible analgesic properties. In Australia, Aboriginal people employed the juice from the raw tuber to heal burns (Webb 1959). Interestingly, the leaf sap was used for similar purposes in Africa, as a healing agent for burns on the Ivory Coast, and the leaf itself as a poultice on abscesses in Senegal (Burkill 1985). In Papua New Guinea the white stem sap was applied to sores, and the leaf then used as a band-aid. A red-leaved variety (wane) was also used for babies (to prevent sores) or in combination with wild tobacco leaves to treat eye infection. In addition the juice from the heated tuber, which dries to a rubber-like gum, could be used to hold wounds together (Holdsworth & Giheno 1975). In Malaysia a healing antibacterial poultice for boils was made from the leaf combined with powdered lime, Ipomoea aquatica (stem paste) and Amaranthus spinosus (leaf ) (Elliott & Brimacombe 1987). Chinese traditions utilised a poultice of crushed fresh Sweet Potato and Dandelions (Taraxacum spp.) on inflamed or poisoned wounds, while the white heart of the tuber was simply crushed and applied to ease breast inflammation (mastitis) or ulceration of the breast (Chang 1989). Some of these uses tend to be supported by studies showing leaf and stem extracts have antibacterial and antifungal properties – however, the activity can vary substantially depending on the type of extract, extraction process and plant variety (Xie 1996; Bruckner 1949). The Sweet Potato (Ipomoea batatas) has a long history of cultivation. It has the advantage of being a short-term crop, ready for harvest within 3–4 months, although some cultivars can take 6 months. The greatest disadvantage is that the tubers do not store well and can be susceptible to insect damage or fungal rot. This can make them bitter and inedible, and liable to become toxic (Burkill 1985).
CONVOLVULACEAE: MEDICINAL BUSH FOODS
In Chinese medicine the Sweet Potato is regarded as an extremely useful remedy for regulating digestive dysfunction. The tuber is seen as having tonic effects on the stomach, spleen and kidneys, and held a good reputation as a convalescent food, as well as being useful for easing seasickness. The tuber and plant greens have been widely recommended for gastrointestinal distress (nausea, stomach dysfunction, diarrhoea). The cooked tuber was taken with honey to ease ‘dryness’ of the intestines with constipation. A decoction of the stir-fried vine (with salt) was used to relieve stomach ache, colic, vomiting and diarrhoea; or prepared as a decoction with alum to alleviate ‘intestinal heat’ characterised by pain and swelling of the stomach, accompanied by dry retching and constipation. The decocted vine has also been utilised to treat vomiting blood (haematemesis) and blood in the stools (Chang 1989). In Papua New Guinea the vine decoction was similarly recommended for stomach disorders (the vine boiled with the leaves of other plants) – as well as for treating asthma. A variety with a reddish brown tuber was said to be effective as a remedy for dysentery (Perry & Metzger 1980; Quisumbing 1951). However, in the Pacific Islands (particularly Hawaii) the Sweet Potato had a reputation as a useful emetic. It was grated, prepared as an infusion with Tistem (Cordyline fruticosa) and infused. This taken to induce vomiting, for example after eating tainted food (Whistler 1992b; Krauss 1979). Sweet Potato has had a diversity of additional medicinal uses: respiratory distress, spleen and kidney disorders, lactation problems, insect bites and various cancers. Indeed, the leaf decoction has been utilised for tumours of the throat and mouth. The infusion makes an excellent thirst-quenching drink for use in fevers: the tuber sliced, scalded, dried and made into a tea (Duke & Ayensu 1985; Perry & Metzger 1980). A Chinese remedy for a feverish condition (‘hot feeling’) affecting the lungs with cough3, decocted the leaf with sugar and Lucky Grass (Reineckia carnea). Another interesting recommendation for night blindness utilised the leaf decocted with pork liver (Chang 1989). African traditions have a couple of additional recommendations that are suggestive of an analgesic effect: the leaves were used in topical frictions to 3 In Nigeria Sweet Potato peelings (macerated) have also been utilised for treating tuberculosis (Ogbole & Ajaiyeoba 2010).
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relieve intercostal (chest) pain, and in a mouthwash or gum massage for toothache. In addition, the pounded leaves have been made into an enema that was used to prevent miscarriage on the Ivory Coast (Burkill 1985). Indonesian healers have also employed finely crushed leaves to relieve the pain of rheumatic joints (Perry & Metzger 1980).
A Vitamin and Mineral Resource of Consequence
Vitamin A has attracted interest for its protective effects on eye function, particularly the prevention of macular degeneration (Chandrika 2010). A recent Taiwanese study has suggested that a high vitamin A intake from greens such as Sweet Potato leaves or the edible Garland Chrysanthemum pictured here (Chrysanthemum coronarium, syn. Glebionis coronaria), native to the Mediterranean and East Asia, could have protective effects against the development of lung cancer4 (Jin 2007).
In general, Sweet Potato leaves have been an under-utilised nutritional resource. They contain a large amount of protein, are rich in dietary fibre (as is the tuber), with soluble fibre predominant in the leaf and insoluble fibre in the stem (Ishida 2000). The young leaves, which contain vitamin C (21–37 mg/100 g), have a reputation for being antiscorbutic. Good levels of β-carotene Leaves of Ipomoea batatas and riboflavin (plus thiamine and niacin), (Sweet Potato). 4 This refers to dietary levels of vitamin A. However, studies of the use of beta-carotene supplements have suggested that there is no benefit in lung or stomach cancer and, indeed, higher levels might be detrimental (Ulbricht & Chao 2010).
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and vitamin E are also present in the leaves – as are some minerals (per 100 g): calcium (1–36 mg), potassium (210–304 mg), phosphorus (38–56 mg) and iron (0.7–2 mg) (Duke & Ayensu 1985). Another study determined that vitamin B2 levels were comparable to broccoli and spinach, vitamin C content was similar to spinach, and vitamin E comparable to parsley, spinach and leeks.5 Ipomoea batatas leaves contain a high level of beta-carotene (743.9+/–35.0 mg/g DW) that have significant potential benefits, particularly for the dietary prevention of vitamin A deficiency which occurs in many poor communities (Chandrika 2010). Other studies have indicated substantial variability in beta-carotene levels. Yellow/purple varieties contain levels (per 100 g) of vitamin A (β-carotene equivalent) that ranged between 35– 5280 mcg in leaf samples (Duke & Ayensu 1986). In addition, the lutein present in Ipomoea batatas leaves is quite high (1,686 mcg/g dw) – with good amounts of the carotenoids neoxanthin (256 mcg/g) and vioxanthin (640 mcg/g) (Chandrika 2010). β-carotene levels in tuber samples can also vary substantially: 112–281 mcg/g (Failla 2009); 204.3–210.3 mcg/g DW (Priyadarshani & Chandrika 2007). Storage conditions are highly influential in maintaining the nutritional integrity of this vegetable. While drying the product did not have a significant effect, prolonged storage can result in lower levels of beta-carotene. It is therefore important that the right cultivar is selected with a good, stable carotene content that is unlikely to deteriorate (Bechoff 2010; Ishiguro 2007). Interestingly, drought stress can influence tuber nutritional components – leading to increased levels of beta-carotene, vitamin C and chlorogenic acid, as well as promoting the antioxidant capacity of some Sweet Potato varieties (Rautenbach 2010). 5 Ishida (2000) provides a comprehensive analysis of the root, stem, stalk and leaf of two Sweet Potato cultivars (per 100 g). Points of additional interest include the potential presence of magnesium (79 mg and 109 mg), higher levels of potassium (357 and 639 mg) and calcium (174 and 187 mg), lower potassium (68 and 36 mg) levels, as well as a small amount of zinc (596 and 885mcg) and copper (431 & 550 mcg). The absorption of iron, which can be present in good amounts (5.5 mg/100 g), would be enhanced by the presence of vitamin C (Ishida 2000).
Orange-fleshed Sweet Potato. In general, orangefleshed tubers contain substantially more beta-carotene, chlorogenic acid and vitamin C than the cream-fleshed varieties. Cooking (heat) can, however, alter the level of these components. Heat can make beta-carotene more bioavailable (which is promoted by the addition of cooking oil). It appears that steaming, frying or baking would be the best cooking methods, with boiling a less attractive option. Some forms of processing can decrease the carotenoid and vitamin C content, although chlorogenic acid and antioxidant capacity may increase, while other studies have shown little overall alteration in phenolic components (Rautenbach 2010; Bengtsson 2009; Tumuhimbise 2009; Truong 2007; Takenaka 2006).
New Research into an Ancient Crop
In the last decade some remarkably interesting research into the health benefits of the Sweet Potato (tubers and greens) has yielded a number of rather surprising discoveries. The leaf and the purple form of the tuber have been traditionally recommended for the treatment of diabetes (Burkill 1985; Quisumbing 1951), and recent studies tend to substantiate these claims. Extracts (leaf and tuber) have shown an accelerating effect on metabolism, as well as antioxidant, anti-inflammatory and hypoglycaemic activity. In addition, studies have indicated a cholesterol-lowing, anti-arteriosclerotic and eyesight-protective potential (Nagai 2011; Park 2010; Li 2009; Chen 2008; Miyazaki 2008; Han 2000; Innami 1998). The leaf flavonoids attracted particular interest as the active components withpotent pharmacological properties6 (Prasanth 2010; Li 2009; Harborne & Williams 2000). 6 There are a lot of variables that can influence the extraction of active principles in an extract. For instance, flavonoid extraction can be significantly affected by solvent (ethanol) concentration, the ratio of solvent to the raw material, extraction time and temperature; 60% ethanol was found to be the most effective concentration for the extraction of both water- and alcohol-soluble flavonoids (Li 2009).
CONVOLVULACEAE: MEDICINAL BUSH FOODS
The Florist’s Chrysanthemum
Ipomoea mauritiana tubers can grow very large, accounting for the name Giant Sweet Potato. (Courtesy: KAW Williams, Native Plants of Queensland, Vol. 3)
Investigations have confirmed substantial supportive effects for Sweet Potato extracts on pancreatic beta cell function (Niwa 2011). A whiteskinned tuber extract sold as Caiapo (a tablet form of powdered tuber) has shown clinical benefits for insulin sensitivity, glucose control and cholesterol levels in type-2 diabetes. A glycoprotein isolated from the cortex appears to exert a major influence on the antidiabetic activity of the extract, although other compounds may also be involved (Oki 2011; Ozaki 2010; Ludvik 2008, 2004, 2003 & 2002; Kusano 2001; Kusano & Abe 2000). A couple of other species have a similar traditional reputation as antidiabetic herbs – Ipomoea aquatica and I. digitata – with studies tending to support their efficacy.7 Ipomoea digitata (this may actually refer to I. mauritiana) tubers have been prepared as a tablet formulations suitable for clinical use (Chandira & Jayakar 2010). Ipomoea mauritiana (tuber root powder) has shown substantial hypolycaemic activity, and a cholesterol lowering effect (reducing LDL cholesterol and triglycerides, raising HDL cholesterol) (Moushumi 2010). Water Spinach (I. aquatica), which is considered to have an ‘insulin-like’ activity, can also significantly reduce glucose absorption, having an effect equivalent to the anti-diabetic drug tolbutamide (Sokeng 2007; Malalavidhane 2003, 2001 & 2000; Quisumbing 1951). 7 Ipomoea nil and I. pes-caprae have also shown experimental hypoglycaemic activity (Khare 2007).
Chrysanthemum flowers are used in Chinese medicine under the name Ju Hua.
Extracts of Chrysanthemum morifolium (Florist’s Chrysanthemum) and Ipomoea batatas contain phenolic components (ellagic acid, caffeoylquinic acid) with strong inhibitory activity against lens aldose reductase (Terashima 1991). This type of activity is used to evaluate compounds that may have protective potential against diabetic complications such as nerve (neuropathy) and eye damage (retinopathy) – and, possibly, anti-asthmatic activity. This is of interest as Chrysanthemum flowers have cellular protective effects that are linked to its antioxidant and anti-inflammatory properties. The Florist’s Chrysanthemum has long been recommended in Chinese medicine for treating feverish problems, hypertensive symptoms (headaches, dizziness), tinnitus (ringing in the ears) and fainting. Externally it was applied to abscesses or sores. Some of these uses are supported by the activity of chemical constituents in the flowers – flavonoids with hypotensive properties – while a volatile oil component has shown anti-febrile activity (Duke & Ayensu 1986)
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Sweet Potato, particularly purple-fleshed varieties, contain polyphenolic components with protective effects against oxidative stress and inflammatory cellular damage.8 Anthocyanins in particular have been linked to anti-atherosclerotic, antihypertensive and hepatoprotective potential with good clinical prospects. The fact that these compounds have shown experimental anti-fibrotic effects in the liver adds support to these uses of Sweet Potato (Hwang 2011; Choi 2010, 2009; Xie 2010; Zhang 2010, 2009; Suda 2008; Shindo 2007).
Ipomoea eriocarpa is found throughout northern tropical Australia. (Courtesy: Helen Pickering, Flora of Zimbabwe)
These cellular protective properties have led to an interest in the anticancer potential of Sweet Potato – focusing on anthocyanin pigments (glucosides of cyanidin and peonidin) and other phenolic components such as caffeic acid, chlorogenic acid, and caffeoylquinic acid in tuber and leaf extracts (Montilla 2010; Truong 2010; Zhu 2010; Li 2008; Kurata 2007; Kaneshiro 2005; Rabah 2004; Hagiwara 2002). In addition, research has shown anthocyanin pigments have antimutagenic properties (Yoshimoto 2002, 2001 & 1999) and radioprotective activity (Xie 2010; Liu 2005; Zhu 2005). Ipomoea aquatica leaf extracts have also shown anticancer (cytotoxic, antiproliferative) potential, which may (in part) be due to phenolic components (including anthocyanins) (Huang 2005; Prasad 2005a & 2005b). 8 Sweet Potato leaves have the highest phenolic acid content followed by the peel, the whole root, and then flesh tissue (Truong 2007). Other studies have shown total polyphenol levels (per 100 g) could vary substantially: tuber (180 mg and 154 mg) and leaf (90 mg and 356 mg), while chlorogenic acid levels were: tuber (21.1 mg and 15.8 g) and leaf (30.1 mg and 47.6 mg). The discrepancy between total polyphenols and cholorogenic acid levels would be due to the presence of other phenolic compounds in the extracts (Ishida 2000).
New areas of research can sometimes yield unexpected results. Indeed, investigations have suggested that purple Sweet Potato anthocyanins (PSPA) could have memory-protective (neuroprotective, antioxidant, anti-inflammatory) attributes with promising potential for the prevention of oxidative stress-induced neurodegenerative disorders, including Alzheimer’s disease (Kim 2011; Lu 2010; Wang 2010; Shan 2009; Wu 2008; Cho 2003). Similar suggestions have been made for the Swamp Spinach (Ipomoea aquatica) (Sivaraman & Mularidaran 2010a & 2010b). This is of great interest, as the anthocyanin compounds from purple Sweet Potato are stable, and have good potential for use as a non-toxic food colouring. Interestingly, additional studies have shown that dietary Sweet Potato can reduce the effects of oxidative stress during exercise. It would also appear to support the immunological status of individuals employing Sweet Potato (tuber, leaves) in their diet (either white or purple skinned varieties) (Chang 2010 & 2007; Chen 2005; Miyazaki 2005). This may also be due, in part, to a polysaccharide component (PSPP: purified sweet potato polysaccharide) (Zhao 2005). There is another avenue of medicinal potential for the genus that appears to merit equally serious consideration. Ipomoea aquatica, I. digitata, I. eriocarpa and I. mauritiana have been recommended as antiepileptic agents for treating seizures (Madhavi 2010; Vijendra & Kumar 2010; Khare 2007). Although investigations of Water Spinach (Ipomoea aquatica) did not show very strong anti-convulsant activity,9 it was suggested that the remedy may work through sedative and neuroprotective effects that could be linked to the phenolic components in the herb (Sivaraman & Mularidaran 2010a & 2010b). This would tend to support diverse traditional uses of the remedy – including the treatment of nervous and general debility in India, and its reputation in South-east Asia as a hypnotic sedative and calming agent for insomnia, stress and headache. In Tanganyika the leaf was combined with a Waterlily (Nymphaea sp. leaf sap) and taken as a sedative for insanity. Vietnamese traditions make similar use of the plant as a sedative, a poultice being utilised for treating ‘febrile delirium’ (Burkill 1985). 9 There is, however, one older reference that does mention antispasmodic activity (Satyavati 1987).
CONVOLVULACEAE: MEDICINAL BUSH FOODS
Water Spinach or Swamp Morning Glory (Ipomoea aquatica)
Ipomoea aquatica, the popular Asian vegetable known as Kang Kong, forms large floating mats in riverine areas. It is also native to the northern regions of Australia although Aboriginal people appear to have made little, if any, culinary use of it. (Images courtesy: Marshman, Wikipedia CC by SA 2.0; JM Garg, Wikipedia)
The sap of the Water Spinach (Ipomoea aquatica) has been regarded as possessing an efficacy equivalent to Scammony (Convolvulus scammonia) as a purgative (Quisumbing 1951), and the vegetable itself can act as a mild laxative. In addition, the plant sap has been utilised as an emetic in opium and arsenic poisoning, and to counteract the effects of drinking polluted water (Austin 2007a; Naples 2005). Water Spinach even has a reputation for being useful for treating worms: ‘the seeds are a strong pesticide killing earthworms, leeches, pig tapeworm and other intestinal parasites’ (Naples 2005). Thus it is not surprising that the herb has been used for gastric and intestinal disorders.
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Indeed, recent research provides support for an anti-ulcerative effect. Extracts not only showed an experimental healing effect on ulceration, but also acted as a gastroprotective agent. This suggests that Kang Kong could be a useful dietary addition to prevent gastrointestinal tissue damage due to chemical insults (Sivaraman & Mularidaran 2008). Investigations also support an antimicrobial effect of the herb; in the Philippines an extract prepared for use as a mouthwash demonstrated activity against Escherichia coli and Staphylococcus aureus (Bhakata 2009; Castillo 1982). The flower buds have been applied as an antifungal agent for ringworm (Burkill 1935). In Myanmar the herb was recommended for treating menorrhagia (excessive menstrual bleeding) and as a tonic, as well as being applied locally as an anti-inflammatory remedy (Ministry of Health, Myanmar nd). Nutritionally, the herb is rich in vitamin C (100 mg/100 g), and is said to be an excellent source of iron, as well as a good resource for calcium and the vitamins A, B and E. It also contains methionine (S-methyl-methionine) (Austin 2007a; Low 1992; Quisumbing 1951).
Sweet Potato Toxins The mould found on rotting Sweet Potato tubers is highly toxic. The relevant chemical investigations are summarised by Selwyn L Everist in the Poisonous Plants of Australia (1981), who noted: workers in Japan and USA showed that when infected by certain mould, fungi or subjected to mechanical or chemical sweet potato Flowering Sweet Potato injury, tubers could produce (Ipomoea batatas).
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A Case of Mistaken Identity
Sweet Potato tubers. (Courtesy: Kim and Forest Starr, Hawaii) the furanoid sesquiterpenes ipomeamarone and hydroxymyoporone. These compounds are related to ngaione from Myoporum [a native tree] and are similarly hepatotoxic to many animals. In some circumstances, especially when the infecting agent is the mould fungus Fusarium solani, further conversion of ipomeamarone takes place to ipomeanine, 4-ipomeanol, l-ipomeanol and 1,4-ipomeadiol, all of which are pulmonary toxic. These compounds, mainly 4-ipomeanol, are responsible for lung injuries observed in field cases of mouldy sweet potato poisoning of cattle. Liver injury was not observed in these cases. Speculation [is] that this may be due to inherent resistance of bovine liver to the longer chain hepatotoxic compounds such as ipomeamarone.
Ipomeanol (specifically 4-ipomeanol) provides an example of how a toxic compound can act as an impetus for drug development. The National Cancer Institute in the United States investigated the use of this chemical as a potential agent against lung tumours. However, clinical studies in 1998 did not show any benefits and established that its use was limited by liver toxicity. Although trials of the drug were later undertaken for liver cancer (advanced hepatocellular carcinoma) it was ineffective. However, this is not the end of the tale. Research has continued to examine analogues that may be more suitable for clinical use (Lakhanpal 2001; Kasturi 1998; Nunes 1998; Rowinsky 1993). While it remains unknown whether some future derivative could be useful, a wealth of knowledge has been gained about the chemical properties of this class of compounds.
Datura inoxia has a large white flower and opens at dusk, hence the name Moonflower. (Courtesy JM Garg, Wikipedia)
White Moonflower, Ipomoea alba, is another nightflowering species whose beautiful flowers are said to be reminiscent of the full moon. (Courtesy: Wikipedia CCA-by-SA3.0)
Sometimes toxicological reactions to a drug can involve some unexpected consequences. There are a few species that go by the common name ‘moonflower’, such as Purple Moonflower (Ipomoea mauritiana) and White Moonflower (Ipomoea alba). However Datura inoxia, which also goes by this name, should not be confused with these vines because its seeds can have significant effects on the nervous system due to their content of tropane alkaloids, which have anticholinergic effects. A report of Moonflower toxicity mentioned an incident where the seeds of Datura inoxia were mistaken for flax seeds and put on a dessert. The hallucinating participant landed in an intensive care unit, flushed in the face and feverish, with tachycardia (fast heartbeat). The main toxic culprit in the plant is scopolamine (Stellpflug 2011).
CONVOLVULACEAE: MEDICINAL BUSH FOODS
Bush Potatoes and ‘Underground Pumpkins’ There are around 50 species of Ipomoea found in Australia, plus a number that have not yet been botanically classified. Aboriginal tribes harvested the root tubers, which were usually baked in an earth oven. Those most commonly eaten are: Ipomoea angustifolia, I. abrupta, I. aquatica, I. costata, I. eriocarpa, I. gracilis, I. grandiflora, I. heterophylla, I. uniflora and I. velutina. A couple of these, which are of particular importance in the drier regions of the continent, have been considered equal to the Sweet Potato in flavour and nutritional value. The Desert Yam (Ipomoea costata) of Central Australia and Western Australia is a slender vine with a shrubby appearance that produces decorative pink flowers with purple-red centres. This fairly widespread species yields numerous large edible tubers (up to 2.6 kg) that are usually roasted on hot coals, although they are also edible raw, with a taste resembling water chestnuts (Crase 2010). The Desert Yam has been widely valued as a staple vegetable by inland communities. It is an extremely useful resource that can be harvested throughout the year. The large, somewhat leathery, leaves were The Grass-leaved Convolvulus (Ipomoea graminea) has been an important food source in the northern tropics. It contains good levels (per 100 g) of carbohydrate (12–34 g) and protein (1–4 g), with some fat and various trace elements: sodium (31–159 g), potassium (293–636 mg), calcium (40–95 mg), iron (0.9–3 mg), zinc (0.7–1.1 mg) – as well as having a high moisture content (Brand Miller 1993). In the Northern Territory three types of tubers were recognised. Plants with long, thin tubers were considered sacred in Arnhem Land. Those suitable for cooking purposes had round, fat tubers or were a large elongated shape (Yunupinu 1995). (Image courtesy: Craig Nieminski, flickr)
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utilised as a form of spinach (Isaacs 1994). The tubers, which are usually quite sweet, have a high moisture content (up to 50%) that makes them a useful water source. This Bush Potato yields three different tuber types depending on growth patterns. In good seasons tubers were found at the end of long runners, as well as at the extremities of the roots. An older, and less desirable, woody tuber was located on the parent plant (Latz 1996). A study of the dietary value of this vegetable has shown that it does not cause the large rises in blood sugar (high glycaemic response) that can be associated with refined products, or even the commonplace potato. Diabetes is prevalent among modern Aboriginal communities and the fact that a bush food has these benefits is of significant interest, providing support for traditional dietary habits (Thorburn 1987). The ‘underground pumpkin’ or Native Sweet Potato (Ipomoea polpha) has a large tuber with similar dietary benefits and flavour qualities to the normal Sweet Potato, although it can develop a somewhat rubbery consistency when cooked. This unique species from the arid regions of the continent has the benefit of being available for harvest throughout the year. It has excellent crop potential in terms of coping with poor soils, producing large numbers of tubers, and growing rapidly. However, it is not common, and even some twenty years ago some serious conservation issues surrounded its exploitation potential: ‘With the assistance of Aboriginal people we now know that it is indeed a rare plant. The species is currently known from only one locality in the Northern Territory, but five stands of a closely related species occur in Queensland. Little is known about the Queensland populations except that they are being reduced by clearing, especially in grazing areas because the leaves are toxic to stock. The taxonomic status of these Queensland and Northern Territory Ipomoea plants is still being resolved’ (Soos 1990–91). Three subspecies have since been identified. Ipomoea polpha subsp. latzii is native to the Northern Territory and has a highly restricted distribution. The Queensland subspecies have a wider range, albeit geographically distinct, with at least 1000 kilometres separating the two populations (as well as the Northern Territory site): I. polpha subsp. polpha comes from the northern part of the state (near Lakeland Downs,
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In Central Australia the Native Sweet Potato has potent mythological associations for the Anmatjirra people linked to strong land conservation practices. Although the tubers were traded locally between tribes it was forbidden to remove the seeds, or the plant itself, from the tribal grounds. Even collecting wood from the area where the plant grew was banned to maintain the environment – prohibitions that ensured its specific growing conditions could be met. Litter cover on the ground and an intact canopy above provide optimum growing conditions. Importantly, the plant is not fire tolerant. Clearing practices seriously disturb the ecology of the mature Mulga community habitat, allowing the encroachment of wire grass and spinifex – which, in turn, makes the land more vulnerable to fire disturbance. (Images courtesy: KAW Williams, Native Plants of Queensland, Vol. 2)
Calystegines: Nortropane Alkaloids
Calystegines were originally isolated from Bindweed (Calystegia sepium), although they were later found in numerous Convolvulaceae species, as well as the Moraceae and the Solanaceae, for example, potato plants (Solanum tuberosum tubers, leaves)10 and the toxic medicinal herb Belladonna (Atropa belladonna). Investigations have established these compounds have antidiabetic,
ranging inland to Hughenden), and subsp. weirana from inland southern Queensland (around Roma, St George, Moonie), where it has been known as ‘Weir Vine’ (Johnson 2006).
Native Sweet Potato (Ipomoea polpha subsp. polpha). (Courtesy: KAW Williams, Native Plants of Queensland, Vol. 4)
Calystegia affinis is a native Bindweed found only on Lord Howe and Norfolk Islands. There are two other Australian species: Calystegia marginata, found in New South Wales, Queensland and Victoria, and C. soldanella, which is more widespread, extending to Western Australia. Another species, the Giant Bindweed of southern Europe, Calystegia silvatica, has become naturalised.
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antiviral and anticancer activity. The glycosidaseinhibitory properties, which are similar to those of castanospermine, australine and swainsonine from the Australian Blackbean Tree (Castanospermine australe), have potential for the development of anti-AIDS drugs (Drager 1994; Molyneux 1993; Evans 2002). Ipomoea polpha seeds also contain swainsonine, as well as calystegine11 (Molyneux 1995). Numerous Ipomoea species have been found to be calystegine-positive – as are various species from the genera Argyreia, Convolvulus, Erycibe and Merremia. Swainsonine is a toxic compound that has been linked to stock poisoning by a number of plants in Australia and the United States, which would explain the toxic reputation of the native Weir Vine, Ipomoea polpha subsp. weirana (Schimming 2005 & 1998).
Calystegia sepium root has long been utilised in Chinese medicine as a tonic, nutrient, demulcent and diuretic remedy. It was ‘said to have the power of cementing bones and tendons, if diligently used as a poultice’ – hence it was known as ‘healing tendon root’ (Stuart 1911). (Image courtesy: E Bjarling, Greenwood Lake, New York) Atropa belladonna contains medicinally important tropane alkaloids. Calystegines (calystegine alkaloids) appear to be derived from similar chemical origins within the plant, that is, from tropane alkaloid biosynthesis (Drager 1994).
10 See also chapter 4 re: calystegines in the potato.
Calystegia sepium.
11 Both compounds were identified in Ipomoea polpha and the Weir Vine Ipomoea sp. Q6 [aff. calobra]), which has now been classified as a subspecies of I. polpha. Only one other Ipomoea species is known to contain these compounds, the tropical American species I. carnea subsp. fistulosa (Schimming 2005).
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A Western Australian evaluation of the prospects of native root tuber crops has focused on the practical potential of a couple of species as marketable commodities (Woodall 2010). The Kulyu (Ipomoea calobra) has crop potential similar to the Bush Potato. The young whitish tubers could be eaten raw although, more commonly, the tuber was baked in hot ashes before use. Nutritionally it was found comparable to Sweet Potato. There appears to be excellent potential: ‘This project has clearly shown that the market would enthusiastically embrace product derived from I. calobra [Kulyu] and that the product could fit within existing vegetable processing, distribution and retail systems, although further research is recommended. This crop offers opportunities for regional and indigenous enterprises.’ Surprisingly, recommendations regarding their viability seem to echo some of the observations made by Burkill, so long ago, of the need to make more such crops accessible: ‘Although this project has shown the commercial prospects for I. calobra to be exceptionally encouraging, the following recommendations are of paramount importance if this species is to become a commercial reality. Future research needs to determine how the cultivation environment can be engineered to facilitate shallow tuber formation and thus the ability of the crop to be mechanically harvested (a key requirement for profitable cultivation)’ (Woodall 2010).
Young Ipomoea calobra tubers. (Courtesy: Dr Geoff Woodall)
A Beach Morning Glory: The Goat’s-foot Convolvulus
Goat’s foot convolvulus (Ipomoea pes-caprae).
Cultivated Ipomoea calobra in raised bed and wild harvested Ipomoea calobra tubers; spade used as scale. (Images courtesy: Dr Geoff Woodall)
Not all Ipomoea species are edible. The Beach Vine, Ipomoea pes-caprae, is among those considered undesirable – cooking (peeling and baking) the tuber usually did little to improve the situation, although at certain times of the year was it said to have more acceptable qualities. The centre part of the thick taproot was the only part worth considering, albeit usually stringy, bitter, irritant and generally considered quite unpalatable, only fit for use in times of famine (Levitt 1981). The root had the added deterrent of purgative potential. Even so, the plant was utilised medicinally and was noted to possess the following attributes: mucilaginous, stomachic, astringent, tonic, alterative, diuretic and laxative.
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Perhaps the most useful recommendation involved the use of the stem juice and pulped leaves as a first aid treatment for wounds. It has a substantial reputation for efficacy in marine stings, such as those from stonefish and jellyfish – as well as being utilised for a range of skin disorders. The leaves have been used locally to ease rheumatic pain and colic, as well as for fluid retention (dropsy) – both applied locally and taken internally for the latter (Low 1990; Satyavati 1987; Cribb 1985; Maiden 1889). Other root crops of interest include the Youlk (Platysace deflexa) and Bloodroot (Haemodorum spicatum). The Youlk has an attractive potato-like tuber, with characteristics that suit it for use as a salad vegetable or in stir-fry dishes –cooked, it has been compared to squash. Bloodroot was not equally acceptable due to its bitter, fibrous texture and the staining qualities of the red pigment (haemocorin). The bulb does have a spicy curry-like character, although its usefulness was limited by the fact that the hot flavour continued to increase in a slow persistent manner, and did not stop once the food was finished. This could easily lead to a misjudgement of the potential intensity of the spice, resulting in a rather unpleasant experience. However, the depth of the red colouring may provide an indication of the potential spiciness of the bulb (Woodall 2010). The following cautionary tale involves Haemodorum laxum, a species with a spicy-hot character, which has also been traditionally utilised by Aboriginal people. In the 1880s Ethel Hassell observed the techniques involved in its preparation: ‘I watched the women smash them up into a slimy looking mass, knead them into flat cakes and put into the wood ashes to bake, telling me the fire took a good deal of the heat out of them. They also eat a little of it raw after a meal as a digestive.’ However, when Hassel prepared a similar stew it was so hot as to be inedible (Hassell 1975).
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Native Bloodroots
Flowering Bloodroot herb, also known as Arsenic Plant (Haemodorum coccineum, formerly H. corymbosum). The Bloodroot plant has a distinctive spicy quality that was observed by Ludwig Leichhardt on his exploratory travels in 1848: ‘The crops of the large cockatoos were filled with the young red shoots of the Haemodorum [H. coccineum], which were almost as pungent as chillis, but more aromatic; the plant abounded on the sandy soil.’
There are around 25 species of Haemodorum native to Australia, although a couple remain botanically unidentified. These Bloodroots, which were named for their rich red colouring, were eaten raw or roasted by Aboriginal people, although not all species appear to be equally palatable. Joseph Maiden recorded the following with regard to Haemodorum spicatum: ‘This is doubtless the plant referred to by Mr. Backhouse [1843] … in his account of the foods of the blacks of King George’s Sound. The long bulb is poor fare, occasioning their tongues to crack grievously; it
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is prepared for eating by being roasted and beaten up with the earth from the inside of the nest of the white ant, or with a red substance found on burnt ground’ (Maiden 1900b). This suggests that the clay could have had a detoxification role, possibly to reduce Bloodroot’s irritant spicy character. However, as the bulb contains only low levels of oxalic acid (certainly much less than is present in rhubarb) the effect is not linked to this irritant. The root of another species, Haemodorum coccineum, which is alkaloid rich, also contains saponins and various minerals (notably sodium, potassium, magnesium, calcium), with quite high iron levels (27 mg/100 g) (Barr 1993).
Amaryllidaceae, should be tried for a red dye, which it probably possesses, similar to an allied North American plant [Lachnanthes caroliniana].’ Haemocorin has shown interesting attributes including anti-inflammatory, antibacterial and anti-tumour potential (Harborne 1999). A couple of species have been employed medicinally. In Western Australia Haemodorum spicatum was utilised as a cure for dysentery (Webb 1948). In the Northern Territory a liquid wash prepared from the root stock of Haemodorum coccineum (crushed and prepared as a decoction) was applied to skin sores. The roots were formerly used by Aborigines as an aperient, and have been proposed as a possible substitute for Jalapa – suggesting they have purgative attributes (Barr 1993). Haemodorum corymbosum was also employed as a snakebite treatment at Charter’s Towers (Webb 1969). Len Webb made the following comment with regard to this species: ‘The roots said to be acrid and bitter when raw, though eaten by Aborigines when roasted … Reputed poisonous to sheep and cattle near Hughenden; if pigs feed on the large roots of the plant, their flesh is said to turn a bright red colour … The roots of all species contain a brilliant red pigment’ (Webb 1948). Certainly the genus appears worthy of serious research attention.
Haemodorum spicatum root. (Images courtesy: William Archer, esperancewildflowers.blogspot.com)
The colouring and spicy flavour of Bloodroot is due to a compound called haemocorin that is both highly soluble and stable in alcohol and oils. This has led to experimentation with its use as a colouring for olive oil and vodka. It also has excellent textile dyeing qualities (Woodall 2010). Not only are the roots suitable for use as a dye substance, the flowers and fruit can make purple-red and red-brown colourings (Barr 1993). Interestingly, in 1880 F.M. Bailey commented: ‘Our species of Haemodorum, a genus of
Lachnanthes caroliniana. (Courtesy: Scott Zona, flickr)
Another plant in the Bloodwort family (Haemodoraceae), the North American Lachnanthes caroliniana, known as Redroot, is a rich source of red colouring matter that includes the
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compounds haemocorin and lachnanthoside. Chelidonic acid, glycosides and naphthalene derivatives are also present (EMEA 2000). The root gained a rather odd reputation based on a remark by Charles Darwin in 1866: ‘The pigs ate the paint-root, Lachnanthes, which colored their bones pink’ (Oxford English Dictionary, 1971). The herb, prepared as a tincture, has been utilised medicinally. Dr Charles Millspaugh (1892) provided the following details: ‘The root was esteemed as an invigorating tonic by the Aborigines [in America], especially the Seminoles, in which it is said to cause brilliancy and fearless expression of the eye and countenance, a boldness and fluency of speech, and other symptoms of heroic bearing, with, of course, the natural opposite after effects. A tincture of the root has been recommended in typhus and typhoid fevers, pneumonia, various severe forms of brain disease, rheumatic wryneck, and laryngeal cough.’ The homoeopathic recommendations for the herb are similar: mental exhilaration followed by ill-humour, vertigo and headache; restlessness, insomnia, coldness, sweat and feverish conditions (throat dryness, fullness and heat in the chest, redness of the cheeks), and eye problems (dull oppressive pain, vision impairment). It was noted to be exceptionally effective for treating a wry-neck with inability to move the head associated with severe pain that radiates to the shoulder (Millspaugh 1892).
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Pacific Islander societies tend to have have slow starchrelease properties. One study found 23 out of 30 foods fell into this category. Wattle seeds (Acacia aneura) and Cheeky Yam (Dioscorea bulbifera) gave very low glycaemic and insulin responses. The Blackbean (Castanospermum australe) and sugarbag honey had similar properties – as did numerous other bush foods. Bunya Pine nuts (Araucaria bidwillii), Sweet Potato, Breadfruit (Artocarpus altilis) and Taro (Colocasia esculenta), which were digested more quickly, were rated somewhat similar to potatoes (Thorburn 1987).
A Future for Bush Foods?
Bush food spices. (Courtesy: jude, www.outbackchef. com.au)
Lachnanthes entry in Materia Medica of Homoeopathic Medicine, Dr SR Phatak (1977).
There are a lot of other bush foods to choose from with dietary benefits – although all too often the complexity of their preparation can be a serious deterrent to their acceptance. Potatoes, corn, white pasta and rice are simply much easier to prepare. Many traditional staples utilised both by Aboriginal and
There has been substantial interest in the development of the bush food industry in Australia. Not only are the Native Sweet Potato or Bush Potatoes of interest, but there are numerous other prospects for crop development (see Smyth 2010; Miers 2004; Forbes-Smith & Patton 2002).12 Most of us would be familiar with the Macadamia (Macadamia integrifolia), and the Australian Marking Nut (Semecarpus 12 See also CJ Williams, Medicinal Plants in Australia, Volume 1.
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australis) could have similar prospects. The Desert Kurrajong (Brachychiton gregorii) is another seedbased product of interest. Wattle seed-based coffee and ice-cream have a particularly good reputation, and Acacia-derived flours (A. aneura, A. colei, A. kempeana, A. murrayana, A. victoriae) also have potential. Bush Tomatoes from a number of Solanum species, especially S. centrale, S. chippendalei, S. cleistogamum and S. ellipticum, are another popular option. Among the diverse offerings of Australia’s bush foods are many that easily substitute for common spices and flavourings: Tasmanian Pepperberry and Pepperleaves (Tasmannia lanceolata), Lemon Myrtle (Backhousia citriodora), Anise Myrtle (Syzygium anisatum, formerly Backhousia anisata), Native Mint (Prostanthera incisa), Desert Lime (Citrus glauca), Finger Lime (Citrus australasica) and Lemon Aspen (Acronychia acidula). In addition there is a remarkable array of unique fruits, some of which are eminently suitable for the production of jams, desserts or chutneys: Quandong (Santalum acuminatum), Wild Plum (S. lanceolatum), Cedar Bay Cherry (Eugenia reinwardtiana), Davidson’s Plum (Davidsonia jerseyana, D. pruriens), Muntries (Kunzea pomifera), Kakadu Plum (Terminalia ferdinandiana), Illawarra Plum (Podocarpus elatus), Burdekin Plum (Pleiogynium timorense), Native Raspberry (Rubus moluccanus), Wild Passionfruit (Capparis spinosa), Bush Orange (Capparis mitchellii), Conkerberry (Carissa lanceolata), Bush Banana (Marsdenia australis, flowers and fruit), Bush Bean (Rhyncharrhena linearis), Bush Melon (Cucumis melo), Rosella or Queensland Jam Plant (Hibiscus subdantta), Riberry (Syzygium luehmannii) and numerous other edible Lillypillies. Native fruits and spices are loaded with antioxidant compounds, giving them excellent potential as healthy additions to the diet. Investigations of the antioxidant potential of native fruits, focusing on phenolic compounds, has shown a high anthocyanin content in Tasmanian Pepperberry and the Illawarra Plum
that was above that of most well-known berry fruits, including Bilberries (Vaccinium spp. cv Biloxi). These compounds are also present in good amounts in the Burdekin Plum, Davidson’s Plum and Molucca Raspberry. Although Muntries and Cedar Bay Cherries had the lowest level of phenolics, their content still rated well (Netzel 2006). Other studies have provided equally interesting results (Konczak 2009): • Outstanding antioxidant capacity of Kakadu Plum and Quandong. Superior antioxidant activity was demonstrated by Tasmanian Pepperleaf, Lemon Myrtle and Anise Myrtle. • Outstanding levels of vitamin C in the Kakadu Plum and Desert Lime. • Vitamin E resources: very good levels in Aniseed Myrtle and Lemon Myrtle, with the levels in Tasmanian Pepperleaf, Kakadu Plum, Quandong and Desert Lime comparable to that found in Avocado. • Lutein, which has particular value for maintaining eye function, was very high in Anise Myrtle, as well as being present in Lemon Myrtle, Tasmanian Pepperleaf, Kakadu Plum, Desert Lime and Davidson’s Plum. • Folate levels were rich in Desert Lime, and good levels were also present in Pepperleaf, Quandong, Kakadu Plum, Riberry and Lemon Aspen. Other bush foods with mineral values of interest are: • High potassium:sodium ratio: Davidson’s Plum. • Selenium and iron: Bush Tomato and Wattleseed. • Iron: Tasmanian Pepperleaf, Quandong, Lemon Aspen. • Magnesium, zinc, calcium: Tasmanian Pepperleaf and Wattle seed; Lemon Myrtle and the Desert Lime were calcium-rich, Anise Myrtle was rich in magnesium, and the Quandong in magnesium and zinc.
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Pretty Purgatives The Genus Ipomoea
Giant Potato, Ipomoea mauritiana, from John Reeves (1774–1856), Collection of Botanical Drawings from Canton, China.
Of the fifty-plus Ipomoea species found in Australia a substantial number have been introduced. There are a few of interest that have been used medicinally both overseas and in Australia. They include Ipomoea aquatica, I. batatas (introduced), I. cairica (introduced), I. carnea (introduced), I. digitata, I. eriocarpa, I. mauritiana, I. nil (introduced), I. pescaprae, I. pes-tigridis (introduced) and I. purpurea (introduced). However, considerable confusion as to their use may arise from the botanical synonyms utilised. For example, Ipomoea digitata and I. mauritiana appear to have been used interchangeably in much of the literature. Ipomoea hederacea has been listed as a synonym for I. nil in some texts. Ipomoea fistulosa is given as I. carnea subsp. fistulosa, while I. macrantha was formerly known as I. violacea in Australian references.
Ipomoea mauritiana by Johannes Scharf, from Nicolai Josephi Jacquin, Plantarum Rariorum Horti Caesarei Schoenbrunnensis Descriptiones et Icones, Vol. 2 (1797– 1804).
Ipomoea macrantha. This attractive tropical species ranges from Western Australia to the Northern Territory and Queensland, extending down the eastern coastline to the Sunshine Coast. (Courtesy Tau’olunga, GFDL, CC-by SA 3.0)
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The fact that recognised pharmaceutical drugs have been sourced from the Convolvulaceae should probably not come as a surprise considering that many plants within the family have cathartic side-effects. A number of native Ipomoea have similar purgative attributes, about which Frederick Manson Bailey (1880) wrote: In the beautiful order of Bindweeds, Convolvulaceae, we find some of our indigenous species are still favourably spoken of as Medicinal plants in other parts of the globe where they are also met with. The roots of the order usually abound in an acrid, milky juice, which is purgative, as for instance, the common purge Jalap, and the stimulating cathartic Scammony. This purgative property is said to depend upon a peculiar resin, but with some this purgative resin is replaced by sugar or starch, and the roots then become valuable articles of food, as in the sweet potato. The first species to notice is Ipomoea paniculata [probably I. mauritiana], a large smooth twining plant with palmately divided leaves, and showy purplish flowers; found on most tropical coasts. The thick fleshy roots of this species are said by Baron Mueller, ‘Select Plants,’ to be edible and deserving of cultivation as a food plant. But in other works the roots are said to be cathartic and used as such in many places where the plant grows. The Queensland habitat is from Rockingham Bay to Cape York. In another of our native plants of this genus, Ipomoea hederacea13, the purgative qualities are in the seeds. The seeds are sold in the apothecaries’ shops of India under the name ‘Kala dana’ (Black seed), and are said to be a quick and effectual cathartic. The seeds are roasted like coffee, powdered, and administered in doses of from 30 to 40 grains, in any convenient vehicle. This plant, which is one of the most beautiful of the genus, is met with in the tropics everywhere. The leaves are usually 3-lobed, and the flower a most delicate light blue; large plants may be seen in some of the gardens about Brisbane.
Indeed, Ipomoea hederacea is only found in Australia as a garden escapee around Brisbane, although some confusion exists in the literature as this name has been misapplied to Ipomoea nil – the seeds of which are also known as Kaladana.
13 This species should not be confused with the naturalised Ipomoea hederifolia (syn. I. angulata), which is a widespread from Western Australia and the Northern Territory, ranging to Queensland and New South Wales.
Flavonoids in Flowers: Ipomoea nil
Ipomoea nil seeds. (Courtesy: Steve Hurst, USDA)
Ipomoea nil. (Courtesy: I Kenpei, Wikimedia Commons)
Ipomoea nil (syn. Pharbitis nil, formerly Convolvulus nil), which is found throughout the tropics, is thought to have been introduced to northern Australia, although this would have occurred prior to European settlement, and so the vine is probably best regarded as being native. It can be found along the coastal regions of Queensland, Northern Territory and Western Australia (north), ranging inland. F.M. Bailey (1880) mentioned it (under I. hederacea): ‘The species so commonly seen trailing over the sandy
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beach from the Richmond River to Cape York, with leaves on long petioles, broadly emarginate, the vines of which are parallel. Peduncles long as leaves, bearing one or two large pink flowers. It is used in Brazil to form a poultice made with the boiled foliage in cases of scrofulous enlargement of the joints.’ The black (Kaladana) seeds have strong purgative properties, although the remedy was said to have an unpleasant taste due to its resin component (Cribb & Cribb 1981). H.M. Burkill (1985) concurred: ‘Their taste is at first sweetish, then acrid and disagreeable’. Ipomoea nil has lovely blue flowers that open in the early morning and turn pink as the day passes. The vivid colour results from flavonoid derivatives in the petals. Blue is linked to anthocyanidins derived from pelargonidin, while cyanidin gives a red-magenta colour, and dephinidin is associated with orange and intense reds. Carotenoids, as well as betalains, tend to be linked to yellow and red flower colours. Betalains, which are characteristic of the Caryophyllales, would perhaps be most familiar as the intense purple colouring of beetroot. There are two types of betalains: betacyanins give red-violet pigments, while betaxanthins are yellow-orange (Tanaka 2010).
Pharmaceutical Purgatives
Pulvis Jalapae from Phillips’ Translation of the Pharmacopoeia Londonensis, 1841.
In the British Pharmaceutical Codex of 1949 the use of Scammony Resin, from Ipomoea orizabensis, was detailed as follows: ‘Ipomoea resin is a drastic purgative, resembling jalap and colocynth in the
Extractum Jalapa from Phillips’ Translation of the Pharmacopoeia Londonensis, 1841.
rapidity of its action. It may cause nausea and vomiting; large doses cause acute gastro-intestinal irritation, with congestion of the pelvic viscera. If absorption occurs it gives rise to cystitis and nephritis. The action of ipomoea resin is greatly facilitated by administration with ox bile or sodium tauroglycoholate. The resin is used with anthelmintics to remove threadworms and roundworms. It is administered as pills or in powders. When prescribed in pills, an equal weight of soap should be added to assist the preparation of the pill mass.’ The effects of Jalap Resin, or Jalapa, from Ipomoea purga were similar: ‘Jalap is a powerful purgative, producing copious watery evacuations. In large doses it causes considerable griping, and its preparation should not be used by those suffering from gastric or intestinal inflammation. Jalap appears to require the presence of bile to emulsify its resin, and the addition of soap increases its purgative power. Its action on the small intestine is very rapid, hence the liquid nature of the stools. Powdered jalap is too bulky for use in pills; for this purpose the resin is preferred.’
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be given for any great length of time, for the depletion finally has a depressing effect on the heart. Though contraindicated in inflammation of the intestinal tube, it may be used when there is inflammation of the biliary apparatus, and when a cathartic is needed at the onset of fevers. The Antibilious Physic and that modification of the compound powder as advised by Locke15 are desirable forms in which to use Jalap. Jalap alone purges in about 3 to 4 hours. Tinctura Jalapae from Phillips’ Translation of the Pharmacopoeia Londonensis, 1841.
When used as an alcoholic tincture the addition of mucilage of acacia or tragacanth (12.5%) to act as a suspension for the resin was recommended. Kaladana (Pharbitis seed) from Ipomoea hederacea could be used as a substitute for Jalap. However, adulteration of the commercial product was a common occurrence – Ipomoea muricata, Crotalaria juncea, Acacia arabica, Peganum harmala and Ocimum basilicum were sometimes sold as Kaladana. Details regarding Jalap (under Exogonium purga) were given by the American Eclectic herbalist Harvey Wicks Felter, who noted the following regarding its irritant potential: Large doses produce violent hypercatharsis, sometimes resulting in death. It is a safe and thorough cathartic when no inflammation of the gastro-intestinal tract exists, and may be used where a derivative action, with full stools, is indicated. In small doses (5 grains daily) it may be employed to relieve constipation due to inactivity of the intestinal glands or where hard fecal masses are impacted in the rectum. Movements are facilitated by the secretion induced. It is a useful revulsive14 in cerebral congestion, and may be used in haemorrhoidal conditions with constipation when a stimulating cathartic cannot be employed. The chief use of jalap is for the relief of dropsy [abnormal fluid accumulation under the skin] from any cause. It is commonly used with cream of tartar, which increases both the cathartic and diuretic effects. It should not 14 In medical terms a revulsive is a counter-irritant agent that acts to promote blood flow to an area and thereby promote circulation. It may also have an anti-inflammatory effect.
Flowering Ipomoea hederacea vine. Henry Burkill mentions that some controversy surrounded the medicinal value of Ipomoea hederacea seeds which, in 1868, were ‘made official in Indian Pharmacopoeia. Their efficacy having been questioned, the Indigenous Drugs Committee made a fresh inquiry and in their second report, where the previous knowledge was confirmed, stated that … there is absolutely nothing to prevent their use for jalap.’ (Image courtesy: SB Johnny, Wikimedia Commons Project)
The South American species that has been exploited commercially as Orizaba Jalap or Mexican Scammony Root is Ipomoea orizabensis. Orizaba was originally used as an adulterant of Mexican or Vera Cruz Jalap (or the resin ‘jalapin’ from Ipomoea purga) but its resin was more ether-soluble than that of Jalap.16 Its properties were similar to that of Scammony resin from Convolvulus scammonia roots. Orizaba Jalap extracted with 90% alcohol yielded a 10–20% complex resinous mixture (65% soluble in either). Mexican Jalap (Ipomoea purga) contained 9–18% resin, extracted from the powdered root by boiling with 90% alcohol. The 15 Ginger was added to the mixture to prevent griping side-effects. 16 Two fractions of importance have been determined from the resin: jalapin (ether-soluble) and convolvulin (ether-insoluble)
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Confection of Scammony, from Phillips’ Translation of the Pharmacopoeia of the Royal College of Physicians of London, 1836.
Ipomoea purga, Mexican or Vera Cruz Jalap, Kohler’s Medicinal Plants, 1887.
Compound Scammony Pill, from British Pharmacopoeia 1867.
concentrated tincture was then poured into water and the precipitated resin collected, washed and dried. Resins sourced from the Convolvulaceae are extremely complex and they could not be isolated in a pure form until recently. Jalap was therefore formerly used as a standardised powder known as Jalap resin or Jalapin (Evans 2002).
Scammony (Convolvulus scammonia) from Kohler’s Medicinal Plants, 1887.
A number of other medicinal plants have been utilised as a source of Jalap. The Indian Jalap (Operculina turpethum, syns Ipomoea turpethum, Convolvulus turpethum) is a tropical viny weed that was an effective
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substitute for the strongly purgative Mexican or Vera Cruz Jalap (Ipomoea purga). It is native to Southeast Asia, India and the Pacific Islands, ranging to tropical Australia, as well as being found in tropical Africa. The vine has attractive white bell-like flowers and distinctive broad heart-shaped leaves. FM Bailey commented: ‘[it was] another large climbing species of our tropical coast, and also of India. It is said that the fresh bark rubbed up with milk is used in India as a purgative. About 6 inches in length of the root as thick as the little finger is reckoned a dose’ (Bailey 1880). Indian authorities noted that the white variety was employed in preference to the black, as the purgative effects of the latter were considered too drastic17 (Kapoor 1990). Ipomoea digitata (syns I. paniculata18, Convolvulus paniculata) has long been valued in Indian medicine as a tonic and rejuvenative remedy. Jalapin is present in the root and, while it doubtless has purgative potential, the herb does not seem to have been utilised in this manner to any great extent. Henry Burkill (1935) provides details of its therapeutic reputation: ‘It is medicinal in India and has been so since Sanskrit times, and the mucilaginous bitter roots are stocked in the bazaars. They are somewhat purgative, and are considered to have a tonic action. They are given for diseases of the spleen, for menorrhagia and debility; as a cholagogue and galactagogue. Apparently the plant has the same medicinal uses in the Philippine islands.’ Other authors mentioned the use of this remedy in a number of recipes. The sundried root, powdered and boiled with sugar and butter had ‘the effect of promoting obesity and moderating menstrual discharge’ (Quisumbing 1951). A confection which combined the powdered root, wheat flour, barley, milk, ghee, sugar and honey, was regarded as having restorative properties 17 There are two botanical sources of the drug known as Nishoth in Indian markets: Marsdenia tenacissima (White Nishoth) and Ipomoea turpethum (Black Nishoth). They could be distinguished chemically as scopoletin was characteristic of the latter. Marsdenia contains a different alkaloid (Joshi 1994). 18 Just to add to the confusion regarding Ipomoea botanical names, I. paniculata was formerly included as a synonym of I. digitata. However, it is now regarded as being synonymous with Jacquemontia paniculata. Both vines belong to the Convolvulaceae, although they are quite different in appearance, with the latter having much smaller white or light purple flowers. 19 There is another traditional aphrodisiac compound preparation that is much more complex: the dried root (macerated 14 times in its own juice) was fried in butter with almonds, quince seeds, cloves, cardamom, nutmeg, shatavari (Asparagus racemosus), gokhru (Tribulus terrestris), Mucua pruriens (seed), muesli etc. and made into a conserve with sugar. This was taken dissolved in milk (Nadkarni 1954).
for ‘emaciated and debilitated children’. In addition, an aphrodisiac prescription macerated the root in its own juice, which was then taken with honey and clarified butter19 (Quisumbing 1951).
Illustration by Johannes Scharf of Ipomoea cairica (under I. stipulacea) from Nicolai Josephi Jacquin, Plantarum Rariorum Horti Caesarei Schoenbrunnensis Descriptiones et Icones, Vol. 2 (1797–1804). In Australia the Railway Creeper (Ipomoea cairica), which is usually found behind beaches or along creeks, is regarded as a weedy native vine although it is possibly a pre-European introduction. It is closely related to the decorative seaside Goat’s-foot Convolvulus (Ipomoea pes-caprae). The bitter tuber and stems of the Railway Creeper were regarded as being edible in Hawaii (Burkill 1985). In Australia, where the plant is known as Mile-aMinute, Aboriginal people also utilised the tuber for food. The plant has some value as a fibre source for making rope or sponges – as well as purgative effects similar to that of a number of other Ipomoea species (Cribb & Cribb 1981).
The Common Morning Glory (Ipomoea purpurea) is an ornamental vine that can be found naturalised in New South Wales and southern Queensland.
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Ipomoea digitata and I. mauritiana have been listed as synonyms, and details regarding their medicinal qualities are virtually identical in many texts. Images of the plant also appear indistinguishable. The literature, in the main, appears to refer to Ipomoea mauritiana, to which the name I. digitata has been incorrectly applied. Identification can only truly be settled by knowing the origins of the plant. Ipomoea digitata is endemic to West India (not Asia or Australia). Ipomoea mauritiana has a more widespread distribution: tropical Africa, Australasia, the Pacific Islands, and Central America. (With thanks to Brendan Lepschi and Robert Johnson for sorting out this tangled botanical puzzle.)
Onion Vine or Indian Jalap (Operculina turpethum)
Operculina Wikipedia)
• •
Dr
Ganesh,
www.
turpethum.
(Courtesy:
JM
Garg,
Onion Vine, Operculina turpethum (formerly Ipomoea turpethum, Convolvulus turpethum) is native to the Northern Territory and Queensland, and is naturalised in Western Australia. Onion Vine tuber has been utilised as a roasted vegetable in Western Australia. Edward Palmer (1883) provided additional details:‘The seeds are large and black, enclosed in a transparent skin, generally three or four, smooth, with the angles rounded. The young buds are eaten raw when the seeds are white. They are very plentiful after the wet season, and are gathered by white people and boiled for peas.’ The fresh seeds of Ipomoea heterophylla could also provide a useful snack, although the latter were avoided when fully ripe (Johnston & Cleland 1948). This could possibly be linked to their purgative potential. As well as the Onion Vine, there are four other tropical Australian species: •
Ipomoea digitata. (Courtesy: ayurvediccommunity.com)
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Operculina sp. Cotton Island, from the Northern Territory, which remains botanically unclassified; Operculina aequisepala and O. brownii from northern Australia (Western Australia, Northern Territory, Queensland); Operculina riedeliana, which ranges from northern Queensland overseas to Papua New Guinea and Malesia.
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Table 3.1 Medicinal uses of Convolvulaceae plants found in Australia with acknowledged purgative attributes Species (distribution) Ipomoea cairica (syns I. palmata, I. tuberculata) Railway or Railroad Creeper Australia: ranges from the northern tropics to Western Australia, South Australia and New South Wales; also found throughout the tropics, from tropical Africa to Asia and the Pacific Islands
Ipomoea mauritiana (syns I. digitata, I. paniculata) Giant Potato Australia: northern tropics; also found in tropical Africa, the Pacific Islands, Southeast Asia and India, Central America. Botanical note: The name Ipomoea digitata has been misapplied to this species in Australia and many other places. It can be quite difficult (if not impossible) to differentiate between these two plants in the literature. Therefore the names are utilised as per the referenced material with notes as is appropriate.
Details of purgative attributes; medicinal uses and investigations Purgative activity Seeds: strong purgative and were used as such in India and Nigeria. The effect was probably due to a mixture of compounds, although muricatin A appears to be the main active component (Burkill 1985). Medicinal use • Crushed leaves: used for treating body rashes, particularly if associated with fevers. The herb had useful absorbent healing qualities which provided an eye remedy in Senegal - a bundle of the plant boiled in water applied as a warm sponge to wash the eyes (Burkill 1985). • Fiji: liquid squeezed from leaves: dysentery. Bone fracture, leaves squeezed and heated and applied locally; plant also used for relief of intestinal cramps (Weiner 1985). Investigations • Extracts: showed strong antibiotic activity, although this was not found to be consistent (Burkill 1985; Watt & Breyer-Brandwijk 1962). • Extracts of the seed and flowers have shown antifungal activity; while the leaves contained ergoline alkaloids (ergosinine, and a mixture of ergocornine and ergocristine) (Satyavati 1987). Purgative activity I. mauritiana • Contains a resin resembling Jalap. • Africa: tuberous root employed as a purgative. This property extends to the leaves, which are not edible, although they have been utilised in soup as a purgative and diuretic remedy on the Ivory Coast (Burkill 1985). I. digitata • Stem and leaf extracts of contain organic acids, glycosidic acids (quamoclinic acid A and operculinic acid A) and a number of resin glycosides, e.g. digitajalapin (Ono 2009; Masateru 2009). • Comment: resin glycosides (Ipomotaosides A–D) from Sweet Potato (I. batatas) aerial parts have shown anti-inflammatory potential (Yoshikawa 2010). This suggests that these resins may have additional pharmacological properties about which we are currently unaware. Medicinal use I. mauritiana • Dried and powdered roots: used as an abortifacient in Senegal, although in other parts of Africa its use was avoided by pregnant women. It therefore seems somewhat odd that the decoction was employed on the Ivory Coast as an enema for female sterility, as well as being taken as a tonic during pregnancy or to avoid miscarriage, and for treating kidney pain (Burkill 1985). • Nigeria: the root was similarly utilised as a tonic, alterative and aphrodisiac. The root stock mixed with palm wine was also used by nursing mothers as a galactagogue (to promote milk production) (Burkill 1985). • Comment: Fresh Sweet Potato plants (I. batatas) have a similar reputation as a galactagogue in northern Peru (Bussmann & Glenn 2010). I. digitata The herb has expectorant, diuretic, demulcent, lactagogue (breast milk inducing) and cholagogue properties, as well as being used for treating fevers, bronchitis, liver disorders and heart weakness (Moushumi 2010; Satyavati 1987). Investigations I. mauritiana • Alcoholic extracts of rhizome had central nervous system depressant effects, anti-amphetamine activity and induced hypothermia (lowered temperature) in mice. However no antiprotozoal, anthelmintic, antiviral, anti-inflammatory, diuretic, hypoglycaemic or cerebrovascular activity was demonstrated (Satyavati 1976). • Later studies confirmed hypoglycaemic and hypocholesterolaemic activity (Moushumi 2010). • Comment: This would seem to indicate the presence of different compounds that can predominate in different forms of extract. I. digitata • Tuber: an ether-soluble fraction of the tuber extract contained substances with hypotensive and muscle relaxant properties. However, an ether-insoluble fraction had opposing effects:
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hypertensive, respiratory stimulant, bronchial relaxant, uterine and smooth muscle stimulant (Kapoor 1993; Satyavati 1987; Matin 1969). • Herb: contains coumarin, which has shown antibacterial (bacteria inhibitory) activity against Pseudomonas aeruginosa and Escherichia coli (Madhavi 2010). • Extracts have shown antioxidant activity and a protective effect on renal function, particularly against gentamicin toxicity (Kalaiselvan 2010; Madhavi 2010; Jagetia & Baliga 2004). Ipomoea nil (syn Pharbitis nil, formerly Convolvulus nil) Ivy or Japanese Morning Glory Australia: northern tropics; also widespread throughout the topics Ipomoea purpurea Common Morning Glory Australia: naturalised in New South Wales and Queensland; native to tropical Africa; cultivated around the world
Merremia peltata Cook’s Vine Australia: northern Queensland, Christmas Island; also found in Madagascar, Seychelles, Australasia, Indonesia, Malaysia, Philippines, French Polynesia. Weedy invasive potential on some Pacific Islands.
Purgative activity In Ayurvedic medicine the seeds have long been utilised as a cathartic, purgative and anthelmintic. For the treatment of constipation the seeds could be powdered and used with other drugs, as a substitute for Jalap (I. purga) (Kapoor 1990). Medicinal use Seeds: utilised medicinally in China for their diuretic, anthelmintic, and deobstruent properties. They were prescribed for dropsy, constipation, as an emmenagogue (to promote menstruation) and as an abortifacient (Burkill 1985) Purgative activity The plant has purgative properties (although the leaves have been eaten in Nigeria) which is attributed to the resin found in the root and stem (4.8% in the latter) (Burkill 1985). Medicinal use The herb was utilised as an anti-syphilitic agent, although it was noted to be ineffective (Burkill 1985). Investigations Extracts have shown variable antibiotic effects in experiments that may have been influenced by growing conditions or chemical variation in the species. Alkaloids are present, mainly in seeds, with lesser amounts in other parts of the plant (leaf, stem, root) (Burkill 1985; Watt & BreyerBrandwijk 1962). Seed (but not plant) extracts have shown a good spectrum of antifungal activity (Kapoor 1993; Satyavati 1987). Seed (but not plant) extract: antibacterial activity (Satyavati 1987). Purgative activity Various Merremia species have been utilised as purgatives in a similar manner to the jalap resins. They include M. peltata (stem sap, tuber) in the Philippines. Medicinal use • Recommended for treating wounds, snakebite, thrush, puerperal (childbirth) troubles, and a few diverse other ills such as cough, diarrhoea and worms. • Leaves: bound on wounds, applied to the breast to treat inflammation, or the diluted stem sap used as eye-drops. An infusion of the stem or root was taken to relieve stomach ache, or the root decoction to alleviate uterine haemorrhage (Perry & Metzger 1980; Burkill 1935). • Fiji: liquid pressed from the leaves was taken, and the leaves applied as a poultice, for treating hernia. The leaves have also been chewed and spat on ‘swellings on the body’ (Weiner 1985). • Papua New Guinea: the herb had a similar healing reputation and leaves were applied to skin sores, or the stem sap to heal heal skin infections (boils) and cuts, including knife and axe wounds – as well as being applied to swellings and sore breasts. Diluted stem sap also taken as a remedy to soothe coughs (including whooping cough) and headache (WHO 2009; Woodley 1991). • Vanuatu: Merremia peltata and Melochia odorata (10 leaves of each plant) leaf juice taken to facilitate childbirth; M. peltata stem juice also drunk in coconut water after the birth to facilitate lactation (Bourdy & Walter 1992). Investigations • Extracts have shown anti-viral (anti-HIV) activity (Yamamoto 1997). • The leaf of a related species, Merremia tridentata, has been utilised for treating herpes in south-west India. It has shown anti-inflammatory activity (Bhandary & Chandrashekar 2011).
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Operculina turpethum (syns Ipomoea turpethum, Convolvulus turpethum) Indian Jalap Australia: northern Australia, ranges to Western Australia; native to India
Purgative activity • Indian Jalap was once listed in a number of official European pharmacopoeias. • Root: contains a glycoside-based resinoid substance, turpethin (containing turpethin, α- and β-turpethin: 4–10%), which has effects akin to those of jalapin, although it was regarded as being a less unpleasant alternative with a milder action (Austin 1981). • The resin content of the roots of Operculina turpethum (8–12%) was comparable to that of Ipomoea purga (10–15%) (Satyavati 1976; Quisumbing 1951). • A related species with similar purgative attributes is native to Brazil and the Caribbean – Operculina macrocarpa (syn. Merremia alata) (Burkill 1985). Medicinal use • Root: not only used for the relief of chronic constipation, it was suitable for treating ascites (abdominal fluid retention), splenic enlargement, rheumatism, gout and paralytic disorders – as well as being a folk remedy for snakebites and scorpion stings (Kapoor 1993; Satyavati 1987; Perry & Metzger 1980). • Stem-bark and/or root extracts: periodic fevers, constipation, flatulence, colic, anaemia, splenomegaly (enlarged spleen), raised cholesterol levels and obesity (Ahmad 2009). Investigations • The remedy was reported to have a rather diverse additional range of therapeutic activity: febrifugal, mild diuretic, antibiotic, anti-inflammatory effects (Kapoor 1993; Quisumbing 1951). • Insecticidal activity of extracts (Haque 2000). • Root extracts: anti-inflammatory, anti-arthritic activity (Satyavati 1987). • The plant has been utilised as an anti-inflammatory and hepatoprotective agent. Root ethanol extract: significant liver protective activity particularly against liver toxins; anti-fibrotic and anti-clastogenic activity (Ahmad 2009; Mukherjee 2009; Suresh Kumar 2006). • Leaf extracts: antibacterial properties (Jahangir 2010). • Stem extracts: antioxidant and protective effects against breast cancer in cancer-bearing animals (Anbuselvam 2007).
A Few Weedy Ipomoea
Ipomoea cairica. This naturalised vine is now widespread throughout Australia, ranging from the tropics (Western Australia, Northern Territory and Queensland), along the east coast to Victoria and South Australia. It is also naturalised in Malesia. Operculina riedeliana. Little appears to be known about this species. The genus is resin-rich and it would possibly possess the purgative attributes resembling Jalap. The bark, leaves and twigs yield a milky juice, and the plant contains tropane and pyrrolidine alkaloids. The aerial parts contain fatty acids, including the fairly rare compound erucamide (Eich 2008).
In addition to the 33 species of Ipomoea endemic to Australia, a significant number of introduced ornamentals have become naturalised (around 17 species). Some are more troublesome than others, particularly in bushland and rainforest, due to their weedy habit and tendency to produce prolific quantities of seed, among them: Moonflower (I. alba), Sweet Potato (I. batatas), Coastal Morning Glory or
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Railway Creeper (I. cairica syn. I. palmata), Pink or Bush Morning Glory (I. carnea), Ivy-leaved Morning Glory (I. hederacea), Red Convolvulus or Scarlet Creeper (I. hederifolia), Purple Morning Glory (I. indica), Obscure or Small White Morning Glory (I. obscura), Yellow Morning Glory (I. ochracea), Tiger’s-foot Morning Glory (I. pes-tigridis), Common Morning Glory (I. purpurea), Cupid’s Flower (I. quamoclit), Littlebell or Aiea Morning Glory (I. triloba) and I. wightii. The latter should not be confused with Wright’s Morning Glory (I. wrightii), which is an American plant that is not found in Australia. Of the weedy introduced species, Ipomoea pestigridis, I. quamoclit and I. triloba can be found around disturbed sites such as roadsides, refuse dumps and abandoned settlements. They often favour the edges of the rainforest, in sunny situations where they can twine up through the large trees. The ornamental escapee Ipomoea hederifolia (syn. I. angulata) has been increasingly expanding into tropical bushland and is often found tangled in an ungainly manner around native trees and shrubs. It has a similar appearance to the closely related Ipomoea quamoclit (with which it
Ipomoea pes-tigridis var. longibracteata, from Curtis’s Botanical Magazine, London, Vol. 145, 1919. The Tiger’s-foot Morning Glory (Ipomoea pes-tigridis) is native to tropical Africa and Asia, ranging to the Philippines and New Guinea. It has also been found as a weed in tropical Australia (Western Australia, Northern Territory and Queensland).
Ipomoea hederifolia.
Ipomoea hederifolia.
Cupid’s Flower or Star-of-Bethlehem (Ipomoea quamoclit).
can hybridise), although it has quite different feathery foliage and its blossoms are inclined to be crimson (or occasionally white). Both plants have a similar distribution in the tropics (Queensland, Northern Territory, Western Australia), ranging along the eastern coastline into northern New South Wales. Ipomoea quamoclit appears to be native to eastern India, although it is now found throughout most of the worlds’ tropics. In India it has been employed as a remedy for bleeding haemorrhoids, while in the Congo the leaves were taken as a somniferic. Webb (1948) mentions that it has purgative attributes and was employed as a snuff – as well as being applied to snakebites. The root of Ipomoea pes-tigridis has a similar purgative reputation that has also been utilised
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as an antibacterial healing herb. It was poulticed on sores and infected skin problems (boils, carbuncles, etc.), in Java and the Philippines, while in Tanganyika it was applied to whitlows. This herb has been used as an emollient for tumours in India, Ceylon and Southeast Asia (Burkill 1985). In addition Indian traditions class the herb as having the following attributes: mucilaginous, stomachic, astringent, tonic, alterative, diuretic and laxative (Satyavati 1987; Maiden 1889).
Ipomoea indica
Merremia quinquefolia.
In the Pacific Islands Ipomoea indica (syns I. learii, I. acuminata) has been used as a purge and the leaves, in some places, as soap (Burkill 1935). This vine is a well-known remedy that was probably introduced by sailors in the early 1800s. In Hawaii a popular herbal medicine called koali was sourced from this plant. The crushed herb or scraped bark was taken as a purgative (alone or with other herbs). Its laxative effects were equally appreciated in Tonga and Fiji. In addition, the root paste has Ipomoea indica is found along the eastern coastline from Queensland to New South Wales, as well as in some parts of Victoria, South Australia (around Adelaide) and Western Australia (south-west).
been used as a soothing application for backache or muscular soreness. In Hawaii a poultice (the plant crushed with added salt) has been applied to fractures to promote healing and encourage blood supply to the injured site – a reputation somewhat similar to that of the Bindweed Calystegia sepium in Chinese medicine (Whistler 1992a & 1992b).
Medicinal Merremia Merremia is a tropical genus whose members have a weedy habit. They have gained a reputation as an urban nuisance as the vines quickly colonise
disturbed sites that accompany new developments and road building, or appear following cyclones. Because of the great similarity of many of the vines within the Convolvulaceae, numerous ‘Morning Glory’ species formerly classified as Ipomoea were later placed in the genus Merremia: Ipomoea aegyptia, I. davenportii, I. peltata, I. quinata, I. quinquefolia and I. tuberosa. Other name changes involve Ipomoea sinuata (now Merremia dissecta), I. chryseides (now M. hederacea), I. cinerascens (M. incisa), I. cymosa (M. umbellata subsp. orientalis), I. flava (M. gemella), I. hirsuta (M. quinata), I. linifolia (M. hirta), I. menispermacea (M. peltata), I. nymphaeifolia (M. peltata), I. pentaphylla (M. aegyptia).20
Merremia dissecta.
of the United States.
Merremia dissecta is a widespread weed of northern Australia found ranging from the coast to inland regions, extending into Central Australia. It is native to the Caribbean and, possibly, some tropical regions 20 Merremia aegyptia, M. quinquefolia, M. tuberosa and M. dissecta are considered naturalised in Australia.
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The leaves and seeds contain cyanogenetic glycosides that give infusions of the plant an aroma of almonds and it has been utilised as a flavouring in bakery products. The roots are alkaloid-rich. The vine has had various medicinal uses: the leaves could be employed as a sedative tisane, taken to ease chest problems or for urinary tract infections. It was also utilised against inflammation, scabies and itching skin conditions. Extracts have shown antibacterial properties. The plant, however, has been responsible for poisoning cattle, probably due to its hydrogen cyanide content (Austin 2007b).
Merremia peltata.
Merremia peltata, from Banks’ Florilegium; drawing by Sydney Parkinson.
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Merremia peltata, which is commonly known as Cook’s Vine, is a native species found in the north Queensland rainforest that can develop a serious weedy habit if given the opportunity. Its lovely white flowers can form a stunning roadside display as it climbs rampantly over the trees, vanishing high into the canopy. This herb has been utilised as a fish poison in Vanuatu (Bradacs 2008).
Magical Lianas: The Realm of the Mind
In the mid-1900s, a couple of the Convolvulaceae from the genera Argyreia and Rivea were involved in a somewhat unexpected discovery. These ‘visionary vines’ were known to be traditionally utilised as hallucinogenic agents. The unusual chemistry of their seeds was eventually linked to that of a fungus known as Ergot – a grain contaminant that had long been responsible for dreadful plagues of poisoning in Europe. Despite its toxicity Ergot had been traditionally utilised in midwifery, and it was from these origins that some remarkably valuable drugs were ultimately developed (Nair 1987; Shawcross 1983; Chao & Der Marderosian 1973). It was the search to synthesise the obstetric drug ergometrine that eventually led to investigations by the Swiss scientist Albert Hofmann. In 1943 an accidental experiment with a fungal derivative called lysergic acid revealed its potent hallucinogenic properties: ‘I suddenly became strangely inebriated. The external world became changed as in a dream. Objects appeared to gain in relief; they assumed unusual dimensions and colors became more glowing. Even self-perception and the sense of time were changed. When the eyes were closed, colored pictures flashed past in a quickly changing kaleidoscope’ (Hofmann 1963). The subsequent chemical discoveries were to have far-reaching, and totally unforeseen, consequences. In 1972 Hofmann recalled the experiment: The nature and course of this extraordinary disturbance aroused my suspicions that some exogenic intoxication might be involved and that the substance with which I had been working, lysergic acid diethylamide [LSD] tartrate, could be responsible. In order to ascertain whether or not
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this was so, I decided to test the compound in question on myself. Being by nature a cautious man, I started my experiment with the lowest dose which presumably could have any effect, taking 0.25 mg LSD tartrate. This first planned experiment with LSD took a dramatic turn and led to the discovery of the extraordinarily high psychotomimetic activity of this compound.
Sub-hallucinogenic doses of LSD were later shown to have anxiety-reducing and anti-depressive properties. However, no other derivatives proved to have any greater hallucinogenic activity, although compounds with a number of valuable pharmacological properties were subsequently developed. These discoveries were instrumental in allowing significant advances in the study of serotonin biochemistry, particularly its role in brain and nervous system functioning – making possible some extraordinary new insights into the body’s biochemistry.
Chemical Puzzles of Ancient Hallucinogens
In the sixteenth century the Spanish invaders in Mexico recorded the use of a sacred plant known as Ololiuqui (Rivea corymbosa now Turbina corymbosa). The seeds were used to enhance visionary experiences. The plant’s chemistry, and its effects, were comparable to that of the ‘Morning Glory’ Ipomoea tricolor (syns I. violacea, I. rubrocaerulea), although the latter was regarded as having a stronger effect than Rivea seeds. The chemical puzzle was eventually untangled when it was determined that the active substances belonged to the same class of compounds as those found in Ergot. The main psychotomimetic (mind-altering or hallucinogenic) compound was found to be lysergic acid amine (ergine), with variable amounts of other related alkaloids: isolysergic acid (erginine), ergo-novine, Ipomoea tricolor.
lysergic acid methylcarbinolamide and some clavine alkaloids (Tyler 1988). The seed embryo, but not the shell, contained the active principles and the total alkaloid content could vary depending on the cultivar. The following figures indicate just how small the alkaloid content can be: 0.035% d-lysergic acid amide, and 0.005% d-isolysergic acid amide, chanoclavine, elymoclavine and ergometrine. It requires 200–300 seeds for an
The popular ‘Heavenly Blue’ Morning Glory cultivar appears to result from the hybridisation of I. violacea with I. tricolor.
Stictocardia beraviensis: ergoline alkaloids (lysergic acid amines, clavines) are present in the Crimson Morning Glory (Stictocardia beraviensis), originating from tropical East Africa, and S. tiliaefolia (S. tiliifolia), a Queensland species that contains calystegines (Eich 2008). The latter has a limited distribution in northern Queensland and the Northern Territory. (Images courtesy: Kim and Forest Starr, Hawaii)
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effect equivalent to about 300 mcg LSD. Studies have established that the lysergic acid amide/ chanoclavine ratio increased as the seeds mature. Ergometrine and chanoclavine were among the compounds present with no hallucinogenic properties (Spoerke & Smolinske 1990).
Table 3.2 Convolvulaceae species that contain ergoline alkaloids Genus
Species
Argyreia Ipomoea
A. osyrensis, A. splendens, A. nervosa subgenus: Eriospermum I. amnicola, I. argillicola, I. asarifolia, I. costata, I. diamantinensis, I. iperati, I. jujujensis, I. leptophylla, I. muelleri, I. pedicillaris, I. pes-caprae, I. phyllomega subgenus: Ipomoea I. orizabensis, I. setifera subgenus: Quamoclit I. aristolochiifolia, I. cardiophylla, I. dumetorum, I. marginisepala, I. minutiflora, I. parasitica, I. tricolor subgenus: Poliothamnus I. argyrophylla, I. hildebrandtii S. beraviensis,, S. tiliaefolia, S. cf laxiflora T. abutiloides, T. corymbosa
Stictocardia Turbina
Silver Morning Glory: A Valuable Traditional Medicine The Silver Morning Glory vine, Argyreia nervosa (also known as Hawaiian Baby Wood Rose) is relatively common in some high-rainfall areas along the Queensland coast. It produces seed with visionary potential – although it would take a lot to get any effect. They contain ergoline alkaloids (up to about 0.5% total alkaloids) and, while their use can induce hallucinations, the side-effects involve nausea, constipation, vertigo, blurred vision and lassitude (Jackes 1992). An anonymous writer quoted in James Dukes’ CRC Handbook of Medicinal Herbs (1985)provided the following description of the use of ‘Wood Rose’ seeds: ‘At first you will feel weak and lethargic. If you have a sensitive stomach, you may get nauseated for about 15 minutes. If so sip a little warm water or mint tea and allow yourself to vomit if necessary. Dramamine … may also help. After this has passed you will feel very relaxed and peaceful
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yet very aware. This state of bliss lasts for about 3 or 4 hours and is followed by a gradual descent to normality except that you will probably feel unusually relaxed and mellow for several days.’ The effects were probably more in the realm of a hypnotic experience, rather than acting as a true hallucinogenic agent (Eich 2008). Importation of the herb is banned in many countries, including the mainland United States. Turbina corymbosa (under Ipomoea cymosa), from Edwards’s Botanical Register, 1843. Argyreia nervosa (syn. A. speciosa) has been known by a number of common names: Monkey Rose, Mile-a-Minute, Silver Morning Glory and Baby Wood-Rose. It has pale violet or pink flowers very similar in appearance to those of the common Morning Glory. The decorative dried fruit clusters have been used in floral displays. This vine, which originates from India, can now be found throughout much of the tropics. It was formerly thought to be native to Australia, although it is now considered to have been naturalised, possibly long ago. More recently it has emerged as an ornamental import with weedy potential along the tropical and sub-tropical coast of Queensland. Another native Australian species, Argyreia soutteri, is unfortunately considered to be extinct. Two closely related native species also found in Queensland were formerly placed in Argyreia: Stictocardia tiliifolia (syn. S. tiliaefolia) and S. queenslandica. (Image on left courtesy: Kim and Forest Starr, Hawaii)
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Argyreia nervosa seeds contain diverse other components and chemical analysis has isolated the following: triterpenoids, flavanoids, steroids and lipids (Srivatasav 1998) – as well as caffeic acid and ethyl caffeate (Agrawal & Rastogi 1974b). While there do not appear to be many studies of the pharmacological properties of the seeds, extracts have shown hypotensive spasmolytic and anti-inflammatory activity (Gokhale 2002; Agarwal & Rastogi 1974a). There is also a report of their use for treating vaginal prolapse in cattle and buffalo (Dhillon 2006). Considering the link with ergoline alkaloids, notably ergometrine, the remedy’s reputation would not be unexpected. The Silver Morning Glory has had a long history of
traditional medicinal use and, in contrast to the hypnotic potential of the seeds, the root and leaves were the main parts employed therapeutically. The plant has been highly valued in Indian herbal traditions. Its primary use has been as an antibacterial, wound healing and anti-inflammatory agent – although it has also gained a good reputation as a sexual and nervous system tonic. It has traditionally been regarded as particularly useful for memory problems and mental fatigue. This is interesting because in the last few years many of these recommendations have been supported by research evidence – which suggest this lovely ornamental vine should be taken very seriously as a herbal medicine that could well have an excellent future.
Table 3.3 Medicinal use of the Silver Morning Glory or Elephant Creeper (Argyreia nervosa syns A. speciosa, Convolvulus nervosus, C. speciosus) and related species Treatment category
Recommendations for use
Substantiating investigations
Antiparasitic
• A. nervosa (Kapoor 1990): A. speciosa (Parveen 1990): • Root powder combined with rice water to Antifilarial (nematicidal) activity against Setaria cervi treat elephantiasis. filaria, which infect cattle. • Guinea worm: infestations were said to respond to the use of the leaf, which helped extraction of the worm.
Anti-inflammatory and anti-pyretic
A. nervosa (Kapoor 1990): • Anti-arthritic to ease joint inflammation: combined with castor oil and milk. • Root paste: applied over rheumatic swellings.
A. argentea (Uddin 2010): • Leaf extract: anti-inflammatory. • Root extract: antipyretic activity. A. nervosa (Modi 2010b): Leaf extract: anti-inflammatory. A. speciosa (Ahlawat 2010; Galani & Patel 2010): Root extracts: hydroalcoholic extracts (not chloroform, acetone or methanol) showed antipyretic activity. A. speciosa (Bachhav 2009): Root powder extract: significant anti-inflammatory activity. A. nervosa (Gokhale 2003): Root extracts: immune stimulatory activity; immunomodulatory against the myelosuppressive effects (bone marrow toxicity) induced by cyclophosphamide (a chemotherapy agent used for treating some forms of cancer including lymphoma and leukaemia).
Metabolic function
A. nervosa (Kapoor 1990): • Alterative (a medicament used to restore or normalise general body functions): powdered root combined with ghee • Root paste: rubbed over the body in an attempt to reduce obesity. A. nervosa (Kumar & Alagawadi 2010): Root extract: antidiabetic remedy. A. cuneata (Chopra 1956): Oral administration of a milk extracts of the leaves for 3–5 days brings about a significant remission of the characteristic symptoms of diabetes.
A. speciosa (Kumar 2011): Root extract: anti-obesity effect in animal studies; hepatoprotective and cholesterol-lowering activity. A. speciosa (Habbu 2008): Root extract: hepatoprotective and antioxidant activity. A. speciosa (Kumar & Alagawadi 2010): Root extract: hypoglycaemic activity in diabetic rats. A. speciosa (Hemet 2008): Stem extract: hypoglycaemic and antihyperglycaemic activity in animal studies.
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Analgesic
A. maingayi (Perry & Metzger 1981; Burkill 1935): Malay Peninsula: root decoction applied externally for the relief of bone pain. A. rubicunda (Perry & Metzger 1981): Malay Peninsula: leaves applied on forehead for headaches, with the juice taken internally. A. argentea (Uddin 2010): Bangladesh and India: treatment of rheumatoid arthritis and colds.
A. argentea (Uddin 2010): Leaf extract: antinociceptive (pain killing activity involving action on pain receptors in the nervous system). A. speciosa (Bachhav 2009): Root powder extract: significant analgesic activity.
Gastrointestinal
A. mollis (Burkill 1935): A. speciosa (Rao 2004): Java: root decoction, in combination with Flower extracts: significant antidiarrhoeal activity. some other herbs (Callicarpa, Anethum and Alyxia), used as a remedy for stomach problems. A. speciosa (Ahlawat 2010a): Root extracts: anorexia, appetite loss, colic, flatulence, ascites dyspepsia, (abdominal fluid retention), haemorrhoids.
Genitourinary and fertility
A. nervosa • Aphrodisiac (Kapoor 1990). • Syphilis treatment (Habbu 2009b). Strangury, diuretic (Vyawahare & • Bodhankar 2009). • Gonorrhoea, strangury and gleet (Subramoniam 2007). A. acuta (Duke & Ayensu 1985; Perry & Metzger 1981): • Diuretic activity: Chinese medicine employed plant decoction for dropsy and tympanites (abdominal fluid or gas retention). • Elsewhere it was used as a bechic and emmenagogue. A. argentea (Uddin 2010): Spermatorrhoea. A. wallichii (Anderson 1993): Thailand: lactagogue, infusion used to stimulate breast milk production.
A. nervosa (Gour & Gupta 1959): The herb is utilised in numerous combinations as a sexual tonic. A. speciosa (Riaz 2010): Combined with other tonic herbs, i.e. Withania somnifera, Mucuna pruriens and Tribulus terrestris. Animal studies have shown positive effects on fertility and reproduction rates. A. nervosa (Subramoniam 2007): Root, flower and leaf extracts: aphrodisiac activity in animal studies (mice); greater proportion of male offspring produced with use of root extracts.
Tonic and neurological – general tonic; brain and nervous system tonic
A. nervosa (Patel 1986): • Herb regarded as a useful tonic for the aged. Used in nervous system disorders for • helping ‘mental dullness’. A. speciosa (Habbu 2009b): Rejuvenating, intellect promoting, brain tonic. A. speciosa (Ahlawat 2010): Root extracts: hemiplegia, nervous weakness, neuralgic pain, cerebral disorders. A. argentea (Uddin 2010): Paralysis, marasmus (severe malnutrition with associated protein deficiency).
A. speciosa (Habbu 2010): Root extracts: adaptogenic, anti-stress properties; studies showed adrenal supportive and antioxidant activity. Flavonoids isolated (kaempferol, quercetin) with adrenal supportive activity. A. speciosa (Habbu 2009b): Root extracts: antiamnesic activity. A. speciosa (Vyawahare & Bodhankar 2009a): Root extracts: anticonvulsant activity. A. speciosa (Vyawahare & Bodhankar 2009b; Hanumanthachar 2007a & 2007b): Root extracts: memory improving (nootropic) effect in mice; anticholinesterase activity. A. speciosa (Galani & Patel 2009): Root extracts: CNS depressant activity; sedative action.
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Antimicrobial wound healing
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and A. nervosa (Kapoor 1990; Quisumbing 1951): • Antiseptic, anti-inflammatory and emollient; used in a wide range of skin diseases. • Leaf: maturative and absorptive attributes; applied to promote the suppuration of boils and carbuncles; used to heal sores, and for the treatment of tumorous growths. • A. speciosa (Vyawahare & Bodhankar 2009): • Leaves applied locally: chronic ulcers, ringworm, and itching skin disorders including ringworm (a fungal infection). Leaves taken internally: boils, swellings. A. argentea (Uddin 2010): Bangladesh and India: boils, gastric disorders, tumours. A. nervosa (Siri 2008): Thailand: leaves used as antibacterial agent for infections and skin disorders. A. fulgens (Chopra 1956): Leaves: antiphlogistic (anti-inflammatory); used in treating skin diseases. • A. malabarica (Chopra 1956): • Leaves: used to promote maturation of boils. • Roots: cathartic.
A. nervosa (Batra & Mehta 1985): Studies of the seed oil showed the main component to be oleic acid. The seed oil had a moderate antiseptic activity against a number of fungi and bacteria. A. nervosa (Modi 2010a): • Leaf extracts: antibacterial (Escherichia coli, Proteus vulgaris, Bacillus subtilis, Staphylococcus aureus) and antifungal (Aspergillus niger, Aspergillus flavus, Candida albicans). • Good additive antibacterial activity shown with Clerodendron infortunatum and Vitex negundo. A. speciosa (Kartnik 2003): Wound healing and anti-inflammatory activity. A. speciosa (Ahlawat 2010b): Root extracts: hydroalcoholic extracts showed a good level of antibacterial activity against Bacillus subtilis, Staphylococcus aureus, Escherichia coli. A. speciosa (Shukla 1999): Antifungal activity: isolation of scopoletin and p-hydroxycinnamate which demonstrated highly potent antifungal properties against Alternaria alternata. A. argentea (Rahman 2010): • Stem extract: good range of antibacterial activity against Gram-positive bacteria (Bacillus cereus, B. subtilis, B. megaterium) and Gram-negative bacteria (Streptococcus aureus, Escherichia coli, Salmonella typhae, S. paratyphae, Pseudomonas sp (I), Pseudomonas sp (II), Shigella sonnei). • Stem extract: excellent antifungal activity (Aspergillus flavus, Fusarium equiseti, Altenaria alternata, Colletotrichum corphori). A. nervosa (Siri 2008): Leaf extracts: potential for use as antibacterial agent against in catfish farms; active against Aeromonas caviae bacteria. A. nervosa (Babber 1978): Antiviral: activity against vaccinia virus, but not against Ranikhet disease virus.
A. speciosa (Habbu 2009a): Respiratory disorders A. speciosa (Habbu 2010): oot extracts: antimicrobial (Klebsiella pneumoniae) and ENT (ear, nose India: wound healing, respiratory disorders • R and throat) (bronchitis), tuberculosis. and antitubercular activity against Mycobacterium A. aggregata (Chopra 1956): tuberculosis; flavonoid sulphates isolated as active components. Leaves made into a paste and utilised • Synergistic activity of extract and flavonoid sulphates externally for treating cough and quinsy. with antitubercular drugs demonstrated. A. nervosa (Kapoor 1990): Leaf juice used for treating ear infections (otitis). A. kleiniana (Vijayakumar & Pullaiah 1998): India: leaves, burned and added to castor oil to make a liniment applied on the throat for tonsillitis. A. mollis (Perry & Metzger 1981): Leaf: the juice was used as eye drops for eyeinflammation; poultice applied to boils.
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Ergot: A Remarkable Tale of a Poisonous Fungus
ease post-partum bleeding. In 1582 Adam Lonitzer provided a very accurate description of a ‘foul-smelling’ Ergot fungus: ‘There are long, black, hard, narrow pegs on the ears [of rye], internally white, often protruding like long nails from between the grains in the ear’. He noted its use to induce pains in the womb, giving the dose as three ‘pegs’ (the sclerotia, around 0.5 g) (Lee 2009a).
The Dread St Anthony’s Fire
Claviceps purpurea, from Kohler’s Medicinal Plants, 1887. Claviceps purpurea is the source of the familiar Ergot of Rye infection, which appears as black ‘growths’ on Rye grass. However, there are other fungi (genera: Epichloe, Neotyphodium and Balansia) that belong to the same family, the Clavicipitaceae, some of which can produce ergoline alkaloids. The plant uses these toxins as a deterrent to insects and grazing animals. Some plants may even derive benefits from the relationship – such as enhancement of their competitiveness, improved root growth, increased drought and mineral stress tolerances (Haarmann 2009).
Historically, the dreadful effects of Ergot toxicity were an all-too-familiar scourge to European communities that would seem to indicate the fungus was too toxic to ever possess any pharmaceutical value. Yet medicines have often been derived from unexpected sources. Similar to a number of drugs which later proved invaluable to the medical profession, the earliest therapeutic uses of Ergot were discovered through the practical experience of local healers. In Europe it was traditionally employed by midwives to assist with labour, acting to promote uterine contractions and
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The story of the toxic effects of Ergot (Claviceps purpurea) is replete with unimaginable suffering. The fungus, which infests rye (and other grains), was responsible for outbreaks of the disease known in medieval times as St Anthony’s Fire Woodcut of St Anthony with – a disfiguring and sufferers of ergotism. agonising form of poisoning that was, in the majority of cases, fatal. However, its history can be traced back much further. As long ago as 600 BC an Assyrian tablet referred to a ‘noxious pustule in the ear of a grain’. Throughout history Ergot plagues devastated European populations, particularly in Germany, France and Russia, where rye crops flourished. In 994 AD some 20,000 people (around half the population) died in the south of France, and a century or so later, in 1129, another 12,000 died in the Cambari region. Britain was not as badly affected as the Continent because the main crop there was wheat rather than rye.21 The disorder ergotismus gangraenosus was characterised by sensations of intense heat and dramatic constriction of the blood vessels, which 21 An indication of this is given in 1930 statistics showing the rye:wheat production ratio (millions of bushels) was 4:1 in Poland and 1:100 in England and Wales (Lee 2009a).
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caused a loss of adequate blood supply to the limbs. This ultimately resulted in gangrene. The highly disfigured extremities became blackened, as if they had been charred by ‘holy fire’. At times the illness reached plague proportions, and in the eleventh century the order of St Anthony was established to care for the tragically crippled survivors. There was also a convulsive form of the disease (ergotismus convulsivus) characterised by excruciating pain that resulted from dramatic changes in nervous system function. The severely afflicted were described as suffering terribly, with profuse sweating, violent retching and ‘shrieking in agony’. Medical historians noted that seizures were not characteristic of the disease in areas where the diet contained large amounts of milk and butter. The proposal was put forward that diets deficient in vitamin A predisposed toward the convulsive form of the disease, although this was never confirmed (Lee 2009a; Burn 1962). Despite a distressing familiarity with its devastating consequences it took centuries before the cause was properly identified, when practical steps could be taken to find a permanent solution. In the early 1700s the link between rye and a fungal infection was suggested, but for the next century outbreaks surfaced periodically. In January 1723, a letter from Jacques de Campredon, the French Ambassador to Russia, gave disturbing and horrifying insights into an epidemic that was sweeping through a region of Russia at that time: Already 20,000 persons have died in the neighbourhood of Nijny. At first they thought it was the plague, but the doctors who were sent there, after having made a careful examination, reported that it was not an infectious disease, but that it arose from bad grain which the people had eaten. The grain is reddish and looks very like tares [a type of weed or plant commonly called vetch], spoilt as far as one can judge by the venomous fogs. As soon as people have eaten this bread they become stupefied, with great contractions of the nerves, so that those who do not die on the same day lose their hands and their feet. These fall off in the same way as they do in this country when hands and feet are frozen. None of the remedies which are used in infectious
diseases do any good to those affected, and only those escape who have had good food and have eaten other bread’ (Burn 1962).
It was not until 1853 that Louis René Tulasne was able to describe the life cycle of the fungus. Soon afterwards (1856) another French botanist, one Monsieur Durien, was able to infect rye flowers with Claviceps spores and the mystery of grain contamination was unravelled. Importantly, it was established that two climatic conditions were essential for this to occur: a wet season allowing germination of the fungal sclerotia, followed by a dry, windy spell that permitted dissemination of the spores to the rye flowers (Lee 2009a). Ergot was regarded with great dread, and justifiably so. Many doctors would not countenance the use of such a dangerous remedy – despite the fact that midwives continued to employ it. One would assume that such a potent drug would have been deployed very carefully. Incorrect administration could easily result in still births and maternal death. There can be no doubt that its unwise use by the inexperienced would have resulted in disability and tragedy. The admonitions of the herbalist Maude Grieve (1931) have a brevity that belie the many errors which preceded the limitations ultimately placed on Ergot’s use in conventional medicine: ‘Its long-continued use is dangerous, resulting sometimes in gangrene, and it should only be used in the hands of fully qualified practitioners’. She also warned that in bleeding disorders ‘its use should be restricted to cases of uterine haemorrhage, as it has been found to raise blood pressure in pulmonary and cerebral haemorrhage’. Until 1808 orthodox medicine took little notice of the properties of the fungus. Indeed, it is quite possible that Ergot-based drugs would never have been developed had its value not been re-discovered in America – albeit its incautious use by untutored medical personnel was to be fraught with tales of disaster and death. A letter to the Medical Repository of New York by John Stearns in 1808 entitled ‘An Account of the Pulvis Parturiens, a Remedy for Quickening Childbirth’22, was to trigger a whole new era in its use. Stearns had learned of the use of Ergot
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from an old woman who had migrated from Germany. She had been using it for several years, with a great deal of success, to facilitate cases of prolonged labour. These details sparked a great interest within the profession. During the 1800s it became readily available on an international scale. The first pharmacopoeia to officially list the drug was that of the United States in 1820 which, fortunately, recommended a standard alkaloid content.23 Ergot entered into the London Pharmacopoeia in 1836. The preparations used elsewhere were not as reliable, leading to significant differences in its efficacy. These discrepancies would not be resolved until the discovery of ergometrine, with the chemistry of Ergot being resolved in substantial detail in the mid to late 1900s (Lee 2009). Stearns’ advice was tragically ignored by many once it came into popular use – despite repeated warnings regarding the consequences of excessive prescribing and an emphasis on the use of restricted doses. By 1822 the physician David Hosack was to comment that Pulvis ad Mortem, ‘death powder’, would be a more appropriate name than Pulvis ad Partum, due to the high rate of infant deaths associated with inappropriate use. Its deliberate use as an abortifacient could be equally catastrophic (Lee 2009a; Burn 1962). A condition known as ‘ergotism’ could also result. This was a form of chronic poisoning characterised by the same symptoms as the plagues familiar in Europe – nervous system malfunction, muscular spasms, cramping, and blood supply deficits resulting in gangrene. A particularly ill-fated discovery was its sedative effects on the central nervous system. This increased the chances of even more widespread medical disasters because it led to Ergot’s indiscriminate use in numerous ‘nervous’ conditions in women: anxiety, hysteria, amenorrhoea (lack of menses) and other menstrual disorders. It was also inappropriately used for treating asthma, as an antihidrotic (to reduce night sweats), and a lactagogue (to promote milk secretion in lactating women). Fortunately, after the disastrous side-effects of the remedy once again manifested, medical practice eventually heeded Stearns’ recommendations. It was restricted to the treatment of post-partum haemorrhage – although one can only
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wonder at the degree of suffering that its incautious use had already inflicted.
Ergota from British Pharmacopoeia 1914.
22 The old name for Ergot used by midwives was Pulvis ad Partum, i.e. powder of birth. 23 The amount of active constituents in the sclerotia can vary considerably: 0.01–1.0% making the dosage extremely difficult to evaluate (Haarmann 2009).
Ergota from British Pharmacopoeia 1867 (note the expanded detail regarding its clinical use in the earlier entry).
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In contrast, the benefits associated with Ergot wisely employed were to prove phenomenal. In 1875 the New South Wales Medical Gazette published an article by a New Zealand medic, Dr WRG Samuels, who wrote of his experiences in ‘Ergot of Rye Combined with Opium in Midwifery’. His words provide an interesting insight into the medical practice of the day: ‘There is one thing very certain, and that is, I have administered the combination of opium with ergot in upwards of six hundred cases, whether in labour or flooding from other causes; and all with excellent results. Since writing the foregoing, I was sent for from a distance of about 20 miles inland, to attend to a middle-aged woman, and was informed that she had been in labour for about two days, with no person but a woman (neighbour) with her.’ He found her highly distressed and administered an infusion of Ergot, after which the pains became stronger. By 3.30 am the woman’s strength began to fail: ‘At this juncture I very much feared losing both mother and child. It being too far to fetch further medical aid, [the] night very dark and raining, I determined to operate at 4am (no chloroform); [and] gave a full dose of opium c. ergot, delivered with a pair of Asherell’s long forceps, [and] saved both mother and child, [who] made a splendid recovery, and that, too, without chloroform, or, in fact, any assistance whatever, save an inexperienced woman. The opium, combined with the ergot, did much to lessen sensitive pain and save both mother and child.’ His words certainly tell of a different era, and of common difficulties with some rather grim overtones: If space and time would permit, I could name numbers of cases showing the benefits derived by the above combination of the two drugs, both in tedious labour, abortions, miscarriages &c. &c. However interesting an autopsy on the body of a poor woman who has died in childbed may appear to the student in medicine, to further his knowledge in morbid anatomy and pathological research, for my own part I would much rather see the mother comfortably in bed, with her darling baby snugly nestled in her bosom, than behold the same person the subject of the dissecting room, or the cold, inanimate manifest clay at a coroner’s inquest.
The Ergot Alkaloids
Ergometrine’s ability to facilitate childbirth and reduce post-partum haemorrhage saved innumerable lives over the centuries – whether used in the form of the powdered Ergot fungus or as an extracted drug. Later, methylergometrine (methergin) was developed, which had the advantage of being twice as active as the parent compound (ergometrine). Ergometrine maleate continues to be listed for use as an anti-haemorrhagic in obstetrics. But the tide of research did not stop there. Since then there have been some extraordinary discoveries, the medicinal and pharmacological value of which cannot be underestimated. The ergot alkaloids were a vitally important starting point for an entire range of invaluable drugs. Albert Hofmann was quite lavish in his praise of its chemical inspiration: ‘The ergot alkaloids have an astonishingly wide spectrum of action, a multiplicity of different pharmacological activities such as is rarely found in any other group of natural products’ (Hofmann 1972). Chemical modification aimed for the development of drugs with a specific range of activity, and this was possibly the only way that Ergot could have been safely used on a wide scale. This resulted in a number of drugs designed to have a selective sphere of action, with a reduction in potential side-effects – the latter being important as many ergot alkaloids induced vomiting.
Ergot Alkaloid History The search to explain the toxic and therapeutic properties of Ergot was to demonstrate the difficult path associated with chemical discoveries and thepersistence required to develop useful drugs. Investigation into the chemical basis of Ergot’s action were initiated in 1875, when a French pharmacist isolated the alkaloid ergotinine. However, the compound was inactive and it took another thirty years before another active substance was isolated in 1906 and named ergotoxine. It was not until 1943 that this substance was shown to be a mixture of ergocristine, ergocornin and ergocriptine – which accounted for the substantial variability in its activity. In 1918 the alkaloid ergotamine was discovered, but its makeup was equally complex
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complexity of Ergot’s chemistry was unravelled, with the eventual revelation that ergometrine (not any of the other alkaloids) was responsible for the traditional obstetric use of the fungus. Even then controversy continued. American researchers called this compound ergonovine, and listed it as as such in their official pharmacopoeia, while the British used term ergometrine.
Ergot fungus on wheat. (Courtesy: JoJan, CC-by-SA 2.0, Wikipedia)
and it took another three decades of investigation to unravel its full chemical structure.24 Initially it was thought to be the same as ergotoxine, but clinical experiments showed a difference between their activity. However, neither ergotoxine nor ergotamine had a substantial oxytocic (uterine contraction) effect. In fact, the water extract of Ergot was more efficacious. In 1935 this puzzle was solved with the isolation of ergometrine, which had significant therapeutic advantages over ergotamine: it was better absorbed, had greater specificity of action in obstetric conditions, lacked cumulative toxicity, and its effects were more rapid. Given intravenously it can stop uterine haemorrhage immediately. However, ergometrine needs to be used carefully as it can result in foetal death, and delay lactation. Overall it took more than a century before the 24 Ergotamine is classed as a mycotoxin that acts by mimicking of the activity of a number of neurotransmitters, notably dopamine, serotonin and norepinephrine. Its profound effect on nervous system function would therefore not be unexpected (Meggs 2009).
Over time studies refined the chemical classification and by the 1970s at least 24 alkaloids had been isolated from Claviceps purpurea. These were then classified into three categories: • the Ergometrine group: ergometrine, ergometrinine; • the Ergotamine group: ergotamine, ergotaminine, ergosine, ergosinine; • the Ergotoxine group: ergocristine, ergocristinine, ergocriptine, ergocriptinine, ergocornine, ergocorninine. It is therefore quite understandable that old Ergot preparations could contain at least twelve different alkaloids and were quite likely to have variable effects. Ultimately, over 200 compounds were identified from Ergot – and not all were alkaloids. The powerful vasodilatory compounds acetylcholine and histamine were present in water extracts, as well as vasoconstrictive agents such as tyramine. Ergotamine and ergometrine could also have vasoconstrictive effects. In addition, bacterial contamination of Ergot could result in the formation of putrescine and cadaverine, compounds that lower blood pressure. This explained why some Ergot extracts (depending on the solvent used) could have a hypertensive effect, while others were hypotensive (Lee 2009a & 2009b). Chemical advances lead to the development of numerous derivatives of therapeutic value, some of which resulted in extraordinary changes to many aspects of medical practice. However, numerous obstacles had to be resolved before successful drug developments could occur. One major problem was the low yield from Claviceps purpurea in cultivation, although high-yielding strains are now available. Eventually a strain located in Portugal, growing on
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Paspalum dilatatum, was found to give excellent yields. It was suitable for use as a raw material for the synthesis of lysergic acid which, in turn, was utilised for drug production (Evans 2002). Today Claviceps fusiformis and C. paspali are utilised for the production of clavine alakloids – with around 10,000–15,000 kg of lysergic acid (legally) produced per annum. Claviceps purpurea continues to be employed for the production of peptide alkaloids, with a production level of 5,000–8,000 kg annually (Haarmann 2009). Ergot was eventually to truly earn the reputation ‘indispensable’, rivalling the greatest medical discoveries ever made from natural products (Wallwey & Li 2011; Lee 2009a & 2009b; Evans 1989; Stadler & Giger 1984, Hofmann 1972): Ergotamine and its derivatives such as DHE • (dihydroergotamine) have been successfully employed in the acute treatment of migraine and cluster headaches, although they are not suitable for long-term preventive use. Additionally, DHE has been utilised in the • treatment of orthostatic hypotension and has venous tonic properties. • DHE (and similar drugs) in combination with heparin have proven valuable as a post-operative preventative for thrombosis and embolism, although their vasoconstrictive properties limit their use, particularly in individuals with peripheral vascular disease, arteriosclerosis and hypertension. Various other products have been developed • that facilitate blood flow to the brain, improve cerebral metabolism, lower blood pressure (antihypertensive actions), and for the treatment of varicose disorders such as chronic venous insufficiency and oedema. They include dihydroergotoxine (codergocrine, ergoloid) for the treatment of dementia and age-related memory loss. Alpha-dihydroergocryptine and bromocriptine (and derivative α-ergocryptine), as well as pergolide and cabergoline, are used clinically for the treatment of early-onset Parkinson’s disease. Bromocriptine (bromocryptine) is a particularly important drug with far-reaching therapeutic effects. It acts to block prolactin secretion (produced by the pituitary gland), thereby reducing lactation. The drug has been used clinically in galactorrhoea (excessive
lactation), as well as infertility and prolactinoma (a prolactin-producing pituitary tumour). Bromocriptine can influence another important pituitary hormone, growth hormone – abnormal levels of which are associated with conditions such as acromegaly, a growth disorder causing tissue overgrowth, with changes that include large hands and development of characteristic facial features. A number of other drug developments originated from this research, including antidiabetic agents (improving glucose tolerance and insulin resistance) and compounds with the potential to prevent weight gain. The use of bromocriptine as an anti-Parkinsonism drug is based on a significant antidepressant activity due to its effect on dopamine levels in the brain. Parkinson’s disease is characterised by abnormally low dopamine levels. However, its use is limited by sideeffects such as dizziness, nausea, hypotension, mental confusion, and the enhancement of female fertility (Holt 2010; Evans 1989; Stadler & Giger 1984 ).
The Genus Claviceps
The fungal genus Claviceps contains around 50 species. In addition to Claviceps purpurea, a number of other species can produce ergoline alkaloids, among them C. microcephala, C. nigricans and C. paspali. There are also various chemical races of Claviceps purpurea, the identification of which is extremely important for pharmaceutical purposes as it can have a significant influence on the type of alkaloid production – as well as the yield. Early Ergot production could vary considerably in activity between batches. The choice of fungal raw materials was made more difficult by the fact that fungal appearances could be somewhat deceptive with inferior-looking samples often being the most highly active. This highlighted the importance of producing commercial supplies from ‘good stock’, that is, using spore-cultures from races known to yield high levels of the desired alkaloids. Botanical refinements in the classification of the genus, as well as chemical studies, have continued to offer insights into Ergot’s chemical potential. For instance, a high-yield strain adapted from a wild grass (Anthraxon lancifolius) to Rye grass has produced 0.5% total alkaloids composed of
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identified in Africa only in 1995. Although it appeared to be less toxic than Claviceps purpurea, it had the potential to cause substantial crop damage. Its dissemination across South America and Australia in 1996 was significant as this was the first report of any Claviceps species outside of Africa and Asia. Of particular concern was the rapidity of its spread – within six months of its detection in Queensland all sorghumproducing regions in that state, and in New South Wales (around 70,000 square kilometres), were contaminated. In 1997 Sorghum Ergot was discovered in Mexico, and rapidly moved into the United States. The chemistry of Claviceps africana is quite different to that of C. purpurea, the primary active alkaloid being dihydroergosine (DHES). Its medical implications remain largely unknown. Australian experiments with contaminated grain showed reduced milk yields in cattle and pigs, and piglets died within a few days of birth because of inadequate milk supplies (Haarmann 2009). Claviceps purpurea, from Dennis E Jackson: Experimental Pharmacology and Materia Medica, 1939. Dr Jackson was Professor of Pharmacology, Materia Medica and Therapeutics in the University of Cincinnati College of Medicine, Cincinnati.
ergometrine, ergotamine, ergocornine and ergocryptine. Interestingly, ergometrine was not naturally produced by the infection of this grass in the wild. Substitutes for Ergot of Rye have included Ergot of Wheat, Ergot of Oats (from Avena sativa), and Ergot of Diss from the reed Ampelodesma tenax (Evans 2002). Sorghum Ergot: A New Grain Contaminant In the mid-1990s a new infestation known as Sorghum Ergot was found as a contaminant of grain crops in many parts of the world. The causative fungus was Claviceps africana,
• The story of Ergot illustrates how potent contaminants can enter the food chain, and the unforeseen medical breakthroughs that can come from such origins. A number of other vegetables in common use have an equally fascinating history associated with their journey from wild produce into fare that is fit for the table. In particular, the Solanaceae is a classification that yields a range of staples such as tomatoes, potatoes and the spicy chilli fruit. Many other species employ some rather fascinating chemical strategies that have given this family a potent reputation for toxicity. There are numerous Australian representatives. Some are quite poisonous while others, although they have not been subjected to the rigours of selective cultivation, have characteristics that well suit them for use as native bush tucker resources.
Chapter 4
CULINARY CURIOSITIES: PSYCHOTIC POTATOES AND TASTY TOMATOES The Solanaceae family is not only famous for medicinal plants, ornamental herbs and trees – it contains a great array of spices, vegetables and fruits. The range is remarkable, with innumerable species yielding produce of great culinary and economic value. Among the most famous are Chilli and Capsicum (Capsicum spp.), Potato (Solanum tuberosum), Eggplant (Solanum melongena), Tomato (Lycopersicon esculentum), the Chinese Lantern or Cape Gooseberry (Physalis alkekengi) and the Winter or Jerusalem Cherry (Solanum pseudocapsicum). There are, however, hidden dangers. Many of the Solanaceae have potent pharmacological properties that have seen their development as drug plants, and there are numerous fruiting species of Solanum with highly variable toxic properties. In particular, the Nightshade category has long held a reputation for being poisonous. This has been primarily associated with the glycoalkaloids that are present in the green fruit, including that of common weedy species such as the European Black Nightshade (Solanum nigrum) and the American Nightshade (S. americanum). Numerous Australian ‘Bush Tomatoes’ are classified in this genus. The native Kangaroo Apples Solanum aviculare and S. laciniatum are associated with similar toxicological concerns. Eating the unripe fruit of such plants can have disastrous consequences. In the majority of species, however, the glycoalkaloid levels become substantially lower during the ripening process – a natural ‘detoxification’ mechanism that renders the ripe fruit edible. Related vegetables that undergo
Kangaroo Apple (Solanum aviculare).
similar developmental changes include the Aubergine (Solanum melongena) and the Cape Gooseberry (Physalis spp.). Even some well-known edible fruit such as the Tomato (Solanum lycopersicum) contain steroidal alkaloids that disappear as the fruit ripens – although in the case of the Tomato, the green fruit appears to be nontoxic. 136
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A Toxic Winter Cherry
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of the Winter Cherry can easily be confused with other edible species. While poisoning is usually limited to gastrointestinal distress (nausea, abdominal pain, vomiting, diarrhoea), symptoms of anticholinergic toxicity can occur (mouth dryness, dilated pupils, difficulty breathing, drowsiness). In particularly severe cases of poisoning, convulsions, coma and fatalities have been known to occur (Shepherd 2004; Parisi & Francia 2000).
Bush Tomato Tales
Bush Tomato, Solanum centrale. (Courtesy: AusEmade Pty Ltd, www.ausemade.com.au)
Winter Cherry, Solanum pseudocapsicum. (Images courtesy: I Kenpei GFDL, CC-by-SA2.1I)
The ornamental Winter Cherry (Solanum pseudocapsicum) from South America, which has become naturalised throughout most of Australia, is a weedy nuisance in some regions. Despite its name, the Winter Cherry has toxic qualities. The plant has typical white Solanum flowers and a deceptively attractive orange berry that contains glycoalkaloids: notably the alkaloids solanidine, solasodine and solanocapsidine, and the glycosides solanine and solanocapsine. The fruit
Bush Tomato (Solanum sp.) shrub, showing purple flowers and green fruit. Kings Canyon, Watarrka National Park, Northern Territory. (Courtesy: Robert Ackerman, Wikipedia).
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In the arid regions of Australia valuable fruit resources from the Solanum genus are collectively known as ‘bush tomatoes’. These include the Bush Raisin (S. centrale), Bush Sultana or Wild Gooseberry (S. ellipticum), the Green or Wild Tomato (S. chippendalei), the Tomato plant (S. esuriale) – as well as S. diversiflorum, S. gilesii, S. orbiculatum and S. lasiophyllum. Some are edible fresh or dried, while others require preparation. These shrubs have been a vitally important resource for many Australian Aboriginal tribes, with some species yielding prolific crops given the right climatic conditions. They tend to bear fruit 12–16 weeks following rainfall, in the cooler seasons. Fire has been used deliberately to enhance the crop as most plants regenerate quickly, and fire also tends to clear out competitive plants such as Spinifex (Peterson 1979).
Desert Staples
Solanum chippendalei. (Image courtesy: Adelaide herbarium, source: G Leach, NT Parks & Wildlife)
Solanum chippendalei. (Image courtesy: CP Campbell, West Australian Herbarium)
A number of desert tomatoes are suitable for longterm storage, which gives them added significance as a resource. The most important are Solanum
chippendalei and S. centrale – the latter being easier to harvest as it has a long-lasting fruit that can dry on the tree and remain edible some months later. The fruit can be ground into a food paste or moulded into round balls with exceptionally lengthy keeping qualities (Peterson 1979). In comparison to the conventional tomato, Solanum chippendalei (samples with seeds removed) showed a higher protein and carbohydrate content (mg/100 g): 1.2–2.6 mg and 15–27 mg respectively (tomato 1 mg and 4.1 mg). Significantly higher levels of some minerals (mg/100 g) were present: sodium 18–36 mg (tomato 4 mg), potassium 419–795 mg (tomato 252 mg), calcium 67–98 mg (tomato 252 mg) – as well as vitamin C 12–59 mg (tomato 22 mg). Green specimens had a lower vitamin C content (19 mg), while the amount in the ripe fruit could be substantial (110–113 mg) – suggesting that they made an important contribution to the diet, particularly when eaten in quantity (Peterson 1979). Importantly, Solanum chippendalei is requires preparation before it can be stored for future use – as DW Carnegie recorded during his travels in the Western Desert in 1896: ‘several wooden sticks on which were skewered dried fruits, not unlike gooseberries; these were hidden in a bush, and are remarkable, for they not only show that the native have some forethought, but that they trade in edible foods as well as in weapons and ornaments’.1 A similar observation was made in 1956 by anthropologist Donald Thomson, who provided a great deal more detail concerning an Aboriginal camp near Lake Mackay: On top of some of the brushwood shelters … reserves of prepared vegetable foods had been left. Some of this had been desiccated and was carefully stored. One of these foods was brown in colour, with the appearance and texture of a mass of pulverized preserved figs and contained numerous conspicuous pale yellow seeds, again suggesting a kind of thick fig paste. It had a half1 The conclusion that trade was undertaken in these food products is debatable, but they were certainly used by many tribes and stored for later use (Peterson 1979).
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sweet, half-tart or acid flavour, but it proved palatable and satisfying, as it was evidently obtained in large quantities even in this drought year, it was probably an important staple food. In the absence of the natives, I was not able to identify the fruit from which this food was derived, but concluded that it was one of the several species of Solanaceae that were seen in flower at this season – some of which, however, were highly poisonous. A quantity of dehydrated or desiccated material was also seen at this same camp, neatly impaled on slender twigs which had been stripped of their bark. This proved to be the dried pericarp, or ovary wall, of another species of Solanum which, in the absence of the inflorescence, I could not identify specifically. The discovery of a reserve of prepared and desiccated vegetable food stored in this way was of much interest, particularly in a drought year and in the face of the belief that is widely held that the Australian Aborigines live from hand to mouth and make no attempt to conserve food (Thomson 1962).
The black seeds of Solanum chippendalei (including the adjacent flesh and mucilage) are extraordinarily bitter and are therefore removed before being threaded on sticks and sundried. When rehydrated they are soaked or pounded up in water and make a thick sweet Outback Tomato Chuttomato paste (Peterson ney. (Courtesy: Robins 1975). Foods, Australia) The ‘native tomatoes’ provide numerous examples of the substantial differences that occur in the fruit of closely related species. Their taste and toxicity can vary greatly. The bitter flavour of some subspecies of the Wild Tomato Solanum orbiculatum discouraged its use by some Aboriginal tribes – while it was regularly eaten elsewhere. Solanum coactiliferum contained an undesirable bitter juice that was squeezed out before the fruit could be used to make a ‘tomato paste’ (Latz 1996). In some places this species was simply considered to be inedible. Solanum hystrix could only be used with preparation, otherwise eating the
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fruit resulted in throat soreness. It could also have an inflammatory effect on cuts. Normally, the calyx and seeds were removed and the pulp made into a cake with mallee root bark (pounded and baked) from species of Eucalyptus. Although the fruit was sometimes eaten without baking, it still required processing and was buried to ferment for a few days (Irvine 1957).
Few Australian species of the Solanaceae have recorded medicinal uses. The roots of the Flannel Bush (Solanum lasiophyllum) were boiled and applied as a poultice to leg swellings (Isaacs 1994). (Courtesy: Dinkum, Wikimedia Commons Project)
The process of ripening usually metabolises the toxic alkaloids into saponins with greatly reduced toxicity. Even so, there are a few native species that retain toxins in the ripe berries. They include Solanum quadriloculatum, S. petrophilum, the Potato Bush or Wild Tomato (S. esuriale), the Devil’s Fig (S. torvum), the Indian Nightshade or Devil’s Apple (S. linnaeanum), S. aculeatissimum (now S. capsicoides),
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and the Thargomindah or Sturt’s Nightshade (S. sturtianum) (Latz 1996; Webb 1948; Everist 1981). A word of caution is needed regarding the potential for culinary confusion between the species. For instance, the highly toxic berries of Solanum quadriloculatum can be mistaken for those of the Wild Gooseberry (S. ellipticum) (Latz 1996). The latter is a species of some importance that ‘is said to furnish small edible green tomatoes all the year around and is a widely distributed species ... numerous enough to furnish food on most occasions and situations’ (Cleland & Tindale 1954). However, few other ‘green tomatoes’ were edible. While the bitter characteristic of the unripe fruits of the native Kangaroo Apples (Solanum aviculare, S. simile, S. lanciniatum and S. vescum fall into this category) is usually an effective deterrent to experimentation, incidents of poisoning have occurred. Even when ripe these fruits may leave a residual burning sensation in the mouth (Peterson 1979). The following comment from Baron von Mueller highlights their problematic potential: ‘The Gippsland tribes collect the fruit of S. vescum eagerly … It has much the appearance of S. aviculare (S. laciniatum Ait.), the Kangaroo Apple, to which species it is, indeed, in habit so closely allied, that superficial observers seeing these plants growing promiscuously will hardly become aware of their distinction’. The green fruit of Solanum aviculare is particularly toxic, thus distinguishing the two species was essential. Joseph Maiden provided additional details: As it is obviously very important that two plants, one of which yields an edible and the other a poisonous fruit, should be clearly distinguished, I add the following notes:– S. vescum differs from S. aviculare in green but not in dark purplish twigs; in sessile, decurrent, somewhat scabrous, and less shining leaves, while those of S. aviculare are distinctly petiolate, and, consequently, not decurrent along the twigs; in the more tender corollas, which are very slightly, but not to the middle, five-cleft, and hardly ever outside whitish; in thinner styles and filaments, the latter not shorter than the anthers; in more acute teeth of the calyx; in almost spherical transparently green berries, with large seeds. The berries of S. aviculare are at all times exactly egg-shaped, of an orange colour, and with seeds but half as large as S. vescum (Maiden 1900).
An idea of the seriousness of incidents of accidental
The Green Kangaroo Apple or Gunyang, Solanum vescum, is a widespread understorey shrub that is found along the eastern Australian coastline, ranging from south-eastern Queensland, to New South Wales, Victoria and Tasmania. It is one of the species that benefits from fire, regenerating from seed after heat exposure. Joseph Maiden (1900) wrote: ‘Its large fruit resembles that of the potato. The fruit when perfectly ripe, which is indicated by the outer skin bursting, may be eaten in its natural state, or boiled and baked. It has a mealy subacid taste, and may be eaten in any quantity with impunity; but until the skin bursts, although the fruit may otherwise appear ripe, it has an acrid taste, and causes an unpleasant burning sensation in the throat (Gunn).’ (Image courtesy: Ken Harris)
poisoning can be illustrated by a case recorded in the New South Wales Medical Gazette of 1872. The culprit was identified as Solanum armatum (now S. prinophyllum). The account, which is graphic in its detail, was recorded by medical practitioner Dr JC Cox. On her arrival home a little girl, Margaret, began acting very strangely: On attempting to reach the room door, all the while staring on the ground vacantly, she again several times turned round and round. The father then began to be suspicious that something was wrong and took her and laid her by her sister, who was also drowsy, on the bed; he though the sun had hurt her. On laying her on the bed she gave a loud screech and threw her arms wildly about; and after lying with her eyes wide open, fixed, and stony, satisfied that she was seriously unwell, the father took her in his arms, where she alternately screeched, hugged him, and stared vacantly. At this stage of the case I was sent for, and
CULINARY CURIOSITIES: PSYCHOTIC POTATOES AND TASTY TOMATOES on arrival – about 7 o’clock – found the child lying insensible on the bed, with the eyes fixed and the pupils dilated. The surface of the body was cold and wet with perspiration; she became violently convulsed after she had vomited freely; the epigastric region was tender to the touch, the mouth parched, and the bowels severely purged.
Her recovery was complicated. Over the next 24 hours she was in great distress and suffered greatly: ‘During the evening she continued in the same insensible state, being violently convulsed every ten or twelve minutes, and passing motions involuntarily. The next morning she seemed weaker, and I was afraid sinking, still insensible and passing blood with her water, and involuntary motions; great thirst; great tenderness over the abdomen.’ It took a couple of days before there was any improvement, during which the episodes of purging, convulsions and unconsciousness continued. It was five days before she began to recover some strength – and ten days before she could sit up in bed. The issue of plant poisoning had triggered some concern. Dr Cox voiced some concern regarding the lack of familiarity many medical practitioners had on the subject of poisonous plants: ‘So little seems to be known of the action of the various plants native of this colony that I have thought the brief history I have given you would be interesting, and draw from members of the profession long resident in the colony some valuable and instructive remarks to others and myself.’
The Forest Nightshade, Solanum prinophyllum (formerly S. armatum). (Courtesy: Peter Woodard)
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Solanum sisymbriifolium
Solanum sisymbriifolium fruit. (Image below courtesy: Leonardo Ré-Jorge, Wikipedia)
The widely distributed Sticky Nightshade or Fireand-Ice plant, Solanum sisymbriifolium, yields a fruit very similar to that of some Australian ‘bush tomatoes’, although the plant is distinguished by prickles on the stem, leaf and fruit calyx. The herb has been used in Paraguay as a diuretic and anti-hypertensive remedy and studies have verified that it had a very strong hypotensive action. The root, which has been utilised as an emmenagogue, can affect fertility. This is interesting because in Africa the Zulu used the root-bark as a remedy for female sterility and to treat impotence. In Argentina there have been reports of horses becoming intoxicated after eating the herb. The fruit contains a haemolytic glycoside, while a number of alkaloids are found in the root – solasodine, solasodiene, solamine, solcaproine and cuscohygrine (Ibarrola 1996a, 1996b, 2000).
The necessity for accurate identification was exacerbated by a number of imported species that had dubious toxicological associations. The Queensland Government botanist FM Bailey, in an 1885 article on ‘Our Naturalised Solanums’, mentioned the confusion that surrounded their edibility. The risk of toxicity was quite apparent: ‘I am induced to bring under your notice the following short descriptive notes on some of the naturalised or supposed naturalised Solanums found near our towns, to assist in their identification
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in the event of some of our medical men investigating their properties. We know the fruit of some said to be poisonous in Europe is eaten by the children of this colony with impunity at times, while at other times the effect has been direful. Dr. Bancroft tells me that in a few experiments which he has made with some of the naturalised species here mentioned, their properties vary considerably.’ The green berries of Solanum seaforthianum have definite toxicity. There have been reports that the ripe fruit also can cause gastrointestinal irritation. Solasodine (0.3%) is present in leaf and stem, as well as in the green fruit (Everist 1981). Solanum sodomaeum is associated with similar concerns, although while it is considered toxic to animals, birds seem to eat the berries without any side-effects (Webb 1948). Toxic reactions appear to be associated with solanine poisoning – sweating, dizziness, dimness of vision, vomiting, purging, dilatation of the pupil, hallucinations and cramping. Not only has solanine been isolated from the herb, it also contains the steroid precursor solasodine, as well as solasonine and solasodamine (Watt & Breyer-Brandwijk 1962).
Solanum capsicoides is an introduced weed from Central America that can now be found along the eastern coastal regions of Australia, ranging from northern Queensland to the central coast of New South Wales. The seed-filled fruit does not appear particularly desirable for culinary purposes – although children have experimented with eating the inner pericarp (skin covering) which has a banana-like flavour. However, there are concerns regarding the plant’s toxicity and its use cannot be recommended (keyes.trin.org.au).
The Devil’s Apple
The Blue Potato Vine, Solanum seaforthianum, an American native grown as an ornamental in the Australian tropics, has spread widely into the countryside as a weedy vine. It has been widely planted for its displays of attractive lavender star-shaped flower clusters, which later develop into bunches of bright red fruit that have a somewhat gritty internal appearance.
Solanum linnaeanum. (Courtesy: Kim and Forest Starr, Hawaii).
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A number of Solanum species were imported into Australia quite early in the history of the colony. A few very quickly established themselves as weeds. One of these was Solanum sodomeum (now classified as S. linnaeanum). In 1880 the botanist FM Bailey mentioned its prevalence in the Australian countryside: ‘The beautiful Solanum sodomeum, Linn., with orange-coloured fruits, is a very common object in our forest country. It is also met with at times in the scrubs, but seems to prefer the former situation. It is often imagined that there are two species of this plant because of the pale or variegated tints of the fruit, but this difference is due to some unfavourable circumstance of its growth. The species is indigenous to the shores of the Mediterranean, and was first grown here as a garden plant.’ The plant has been widely used as a folk medicine in South Africa. The fruit or leaf juice was used for treating skin diseases, and extracts (of leaf, stem and fruit) have displayed antibacterial properties. The fruit even provided a ringworm remedy for cattle and horses. Chewing the root extracted a juice that was swallowed as a remedy for colic, or spat on wounds to promote healing. The leaf and fruit have been employed as a diuretic for treating dropsy (as was the root), cystitis (urinary tract infection), and as a cough remedy (Watt & Breyer-Brandwijk 1962).
The Medicinal Tomato
The Tomato is classified in the genus Lycopersicon, which contains only seven species that trace their wild origins from South America and the Galapagos Islands. Botanically, the differences between this genus and Solanum are minor – albeit Solanum is far more vast and diverse. Indeed, one of the synonyms for the Tomato is Solanum lycopersicum.
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The Tomato has been esteemed for its medicinal and nutritive attributes since ancient times. Chinese medicine regarded the sweet and acidic fruit as being beneficial to stomach function. Indeed, the dietary use of the Tomato as a remedy involves some interesting traditions. It was said to be useful for healing gastric ulcers. One recipe utilised sliced tomato mixed with a pickled lemon and honey, which was taken several times daily for three weeks. Ulcers in the mouth were treated with a mixture of fresh fish and tomatoes (cooked together), while for bleeding gums (gingivitis) fresh tomatoes were eaten. Tomato juice and Watermelon juice were mixed and drunk regularly for diabetes – or a soup was prepared from Tomato combined with pork pancreas, oil and salt. A decoction of the root, stump and old leaves could be taken to relieve toothache, or used as a wash for treating chilblains. The stem (including the leaves) was also used as a wash for swollen, poisoned skin problems (Chang 1989). In Indonesia, pulverised tomato leaves were even applied to the face as a cooling remedy for sunburn. In Indochina the fruit was regarded as having laxative properties. It has been utilised for treating phthisis (tuberculosis), typhoid fever, ophthalmia (eye problems), otitis (ear infection) and gravel (urinary tract stones) (Perry & Metzger 1981). Tomato (pulp and juice) has long been considered useful for blood purification and, via the promotion of gastric secretions, was said to facilitate digestive function. According to Eduardo Quisumbing (1951), Tomatoes were worthy of high praise: they are also considered to be an intestinal antiseptic as they have a cleansing effect in the enteric portion of the alimentary canal. They are said to be useful in cancer of the mouth – ‘nurses sore mouth’ – etc. Tomatoes stimulate a torpid liver and are beneficial in … dyspepsia. They are invaluable to those who have a tendency to biliousness as they promote the flow of bile, and also are a great help in cases of bronchitis and asthma. Briefly, the medical and food value of tomatoes may be stated thus: (a) Tomatoes are the richest in vitamins of all foods;
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(b) they are the most wonderful and effective blood cleanser of all foods known to man; (c) they are the richest of all vegetables in the natural health acids which keep our stomachs and intestines in condition; (d) they are the most extraordinary corrective for kidneys, being a gentle natural stimulant which helps to wash away the poisons which cause disease and contaminate our systems.
Of course, those with an intolerance to the Solanaceae would have to forgo the pleasures of this edible wonder.
Carotenoid Complexities
Tomatoes have substantial antioxidant value and are rich in
(e.g. lycopene and α-carotene), as well as a closely related classification, the xanthophylls (e.g. lutein, zeaxanthin).3 Beta-carotene (which is widely found in vegetables) is particularly useful as can be converted to vitamin A in the liver – unlike lycopene, which cannot. However, the latter has attracted special interest due its strong antioxidant properties and anticancer potential. Some Tomato varieties are naturally rich in the compound and, as the fruit ripens, the lycopene content increases. 2 Other good sources of vitamin A include fish liver oils (cod, salmon, halibut), green leafy vegetables, liver, egg yolk, apricots, mint and kholrabi. 3 Over 600 different carotenoids have been identified.
Lycopene in Tomatoes
Lycopene is the most abundant carotenoid in Beefheart Tomato. (Courtesy: Dominik Hundhammer, München, via Wikipedia CCSA 3.0)
folate, the vitamins C and K, potassium, and carotenoids – particularly lycopene (as well as minor amounts of phytoene, phytofluene, zeta-carotene, gammacarotene, β-carotene, neurosporene and lutein). Other components, present in smaller amounts, include vitamin E, various water-soluble vitamins, trace elements (copper, iron and chromium), chlorogenic acid, flavonoids (rutin), plastoquinones and phytosterols (Friedman 2002). (Image on left courtesy: FoeNyx, Wikimedia Commons)
The potential of the Tomato as a medicine remained largely unappreciated until investigations discovered that it contained carotenoids – a pigment that imparts the vibrant red colour to the fruit. The general term ‘carotene’ has been used to describe a mixture of all the carotenes, although β-carotene does tend to naturally predominate. Over time, investigations have revealed the true complexity of this classification, which requires some clarification. Vitamin A was discovered in the early 1900s2, followed by carotenoids
Watermelon slices. (Courtesy: Keith Weller, USDA)
ripe tomatoes, comprising around 80–90 per cent of the pigment present, with negligible levels of other carotenoids (α- and β-carotene, lutein, β-cryptoxanthin). While lycopene levels are highest in tomatoes (ranging from 0.72–20 mg/100 g), this compound is also present in reasonable levels (per 100 g) in watermelon (2.3–7.2 mg), pink grapefruit (0.35–3.36 mg), guava (5.23–5.5 mg) and papaya (0.11–5.3 mg). Lycopene levels increase as tomatoes mature. The average level (per 100 g) is around 3–5 mg, although some varieties can be substantially higher: 9.27 mg (whole tomato fruit) and 15 mg (deep red varieties), while yellow varieties were much lower (0.5 mg). Some cultivars have
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exceptionally high levels: 30.16 mg (full red ripe VT-145-7879) and 54.33–70.21 mg (Canary Island type fresh tomato). Thus the rich red colour that is so attractive to shoppers indicates the presence of good levels of lycopene in the fruit. In addition, the skin and pericarp are the parts richest in lycopene (skin 53.9 mg – in comparison to pulp 11 mg) – although because the skins and seeds are discarded in many processing strategies, up to 80–90 per cent of the total lycopene present in the whole ripe fruit can be lost (Shi & Le Maguer 2000). A growing volume of research shows carotenes to have specific, and significant, health benefits (Osiecki 1998): • B eta-carotene is an important dietary component. It has been found useful for degenerative disorders, photosensitivity, cataract, cardiovascular problems (atherosclerosis, high cholesterol levels), HIV infections, cystic fibrosis, cancer, stress and chemical exposure (pesticides, radiation, chemotherapy, smoking, surgery). • Vitamin A has equally valuable therapeutic attributes, having been utilised in the treatment of diverse immune and inflammatory disorders: joint disease (arthritis), respiratory tract disorders (bronchitis, asthma, emphysema), skin problems (eczema, acne, psoriasis), gastrointestinal disorders (coeliac disease, Crohn’s disease, ulcerative colitis, duodenal and gastric ulcers), genitourinary tract problems (nephritis, cystitis), cervical dysplasia, multiple sclerosis, tinnitus (ringing in the ears), mouth and gum disorders, pancreatic and gall bladder diseases, diabetes, infectious conditions (colds, influenza, viral meningitis), AIDS, tumours and cancer. Vitamin A deficiency has been linked to • proliferative and immune disorders with effects on numerous body systems: poor bone growth, poor immunity, impairment of taste and smell, growth retardation, delayed wound healing, sinus problems, skin and hair dryness. Vitamin A is a component of adrenocorticoid and steroid hormone synthesis. Levels will be compromised
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by air pollution, chemical exposure (chlordane, copper, cadmium, dieldrin, DDT, smoking), stress, athletics, diarrhoeal disorders, and diabetes.
Tomato Antioxidants
The discovery that the antioxidant properties of β-carotene were significantly less than those of lycopene redirected attention towards the latter, which then became the focus of substantial research interest. Lycopene’s effects were found to be quite different from those of other carotenoids, with the potential to influence different disease processes. The protective effect of carotenoids against sunlight damage in skin cells has been of particular interest. Indeed, a combination of carotenoids and vitamin E has shown significant healing and protective effects on skin erythema due to ultraviolet light exposure. The fact that β-carotene levels remained unchanged during exposure to ultraviolet radiation, while lycopene levels were considerably reduced, implies that lycopene was more intimately involved in protecting the skin against sun damage (Shi & Le Maguer 2000; Stahl 2000, Lee 2000; Beecher 1998; Regtop 1998; Wohlmuth 1997). Lutein and zeaxanthin mixtures have also shown antiinflammatory and ultraviolet protective effects with potential to prevent skin damage and enhance tissue repair (Gonzalez 2003). In addition, lycopene has shown a protective effect against the development of atherosclerosis and has been associated with a lowered risk of coronary heart disease (Agarwal & Rao 1998; Shi & Le Mageur 2000). There is an inverse relationship between the level of phenolics and carotenoids in the Tomato. Investigation of the Tomato’s polyphenolic components (i.e. the flavonoids naringenin, rutin, rutin-pentoside; and the phenolics chlorogenic and caffeic acids), linked a low carotenoid content (i.e. lycopene, β-carotene) to higher levels of polyphenols in the fruit – which consequently had a more powerful antioxidant potential. The antioxidant polyphenol naringenin, which is found in good amounts in tomatoes, has shown cholesterol-lowering, antiulcerogenic and anti-oestrogenic properties. It can modify the metabolism of xenobiotic substances. Importantly, naringenin was bioavailable when cooked tomato paste was added to meals. While processing tomatoes reduced the naringenin concentration, the levels of chlorogenic acid and lycopene were increased – attesting to the
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complexity of the changes that occur during the cooking process (Re 2002; Bugianesi 2002; Minoggio 2003).
A Matter of Bioavailability Leggo’s Tomato Paste. (Courtesy: Simplot Australia)
Bioavailability is a particularly important concept for evaluating the benefits of nutrients in the diet. Even though a nutrient may be present in high amounts in various foods, digestive and metabolic processes can significantly alter its practical effects. Unlike many vitamins, carotenoids, such as lycopene, are heat stable and can withstand processing without loss of activity. Indeed, tomato paste was found to be a better source of lycopene than raw tomatoes. While the lycopene from unprocessed tomato juice was poorly absorbed, boiling the juice and adding 1 per cent corn oil resulted in a significant increase in bioavailability.4 This was because lycopene is fat-soluble and the presence of a lipid promoted its absorption. The good news for food manufacturers is that lycopene, unlike many water-soluble and heat-sensitive vitamins and minerals, is not lost in cooked or processed foods. Indeed, processing (grinding, blending) and cooking (heat treatment) have even been shown to increase the bioavailability of vegetable carotenoids (Shi & Le Maguer 2000; Wohlmuth 1997). Supplementation regimes aimed at evaluating bioavailability have also shown increases in blood serum levels that are directly linked to the source of the carotenoids (Olmedilla 2002): • carotene-rich palm oil: α-carotene (14-fold increase) and β-carotene (5-fold increase); • tomato paste: lycopene (2-fold increase); • marigold extracts: zeaxanthin (levels doubled) and lutein (5-fold increase). 4 The type of oil appears to be important. Studies have shown that olive oil, which contains phenolic antioxidants, can enhance the oxidative activity of lycopene in plasma. Sunflower oil does not (Friedman 2002).
The α-carotene and β-carotene content of other vegetables can similarly be favoured by cooking processes. For example, lower blood plasma carotenoid levels were associated with raw carrots and spinach in Carrot slices. comparison to cooked (heat-treated) vegetables in the diet. The difference was quite significant – with the processed food rating around three times greater than the raw product. Pureed or powdered carrot preparations were likewise a superior source of utilisable carotenes. Additionally, the fibre content of raw vegetables can reduce the bioavailability of carotenoids (Edwards 2002; Thurman 2002; Rock 1998; Paetau 1998).
Anticancer Carotenoids
Antioxidants have become a focus of research due to their role in the prevention of inflammatory disorders, cancer, cardiovascular disease, and the various degenerative problems associated with ageing. Vegetables are an important resource because they contain interactive complexes of antioxidant and nutritional substances. Incorporation of tomatoes into the diet appears to have valuable cardioprotective potential that is linked to their lycopene and β-carotene content. Dietary carotenoids may even be associated with a reduced risk of developing angina pectoris (heart pain) and other aspects of coronary artery disease (e.g. cholesterol deposition in the arteries). Tomatoes appear to have a general anticancer effect in the body. Numerous studies have suggested that there is a link between a high intake of tomato products and dietary anticancer benefits.5 Antioxidant compounds can have important 5 Willcox 2003; van den Brandt 2003; Osganian 2003; Giovannucci 2002; Lu 2001, Liu 2001, Dwyer 2001; Bhuvaneswari 2001; Hulten 2001; Kotake-Nara 2001; Cristoni 2000; Nishino 2000; Norrish 2000; KlipsteinGrobusch 2000; D’Odorico 2000; Michaud 2000; Knowles 2000; Ford 2000; De Stefani 2000a, 2000b, 2000c; Bub 2000; Tavani 1999; Kohlmeier 1997.
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benefits for maintaining cellular integrity by preventing the oxidative damage to cellular DNA that is implicated in the development of cancer – which is of interest because lycopene has double the antioxidant activity of β-carotene and over 10 times that of α-tocopherol. The inhibition of cancer cell growth by lycopene has attracted substantial research attention, which has confirmed its benefits in diverse cancer cell lines, notably breast, endometrial, lung and white blood cells. However, it should be noted that while lycopene appears to be a major player in the anticancer activity of tomatoes, the benefits of the whole fruit outweigh the use of pure lycopene. This is suggestive of a synergistic relationship between the diverse other antioxidants that are present in tomatoes (Friedman 2002; Shi & Le Mageur 2000; Wohlmuth 1997): • A diet rich in carotenoids, particularly α-carotene and lycopene, has shown potential benefits in the prevention of lung cancer. • Tomato juice has demonstrated immunomodulatory properties that may be linked to an anticancer effect. • Studies have suggested that tomato-rich foods, and lycopene in particular, may reduce the risk of cancer of the entire digestive tract (oral cavity, pharynx, larynx, oesophagus, stomach, colon, rectum), pancreas, bladder and the prostate. • Tomato sauce appears to help reduce the risk of prostate cancer – albeit the level of the protective effect has been debated. • Lycopene was found to reduce the risk of developing breast cancer. • It is possible that low levels of lycopene in the diet may even be a contributing factor to the development of cervical, bladder and pancreatic cancers. Other investigations also noted the anticancer • potential of carotenoids such as zeaxanthin, lutein and β-cryptoxanthin (particularly the latter). Selenium, bioflavonoids (i.e. quercetin, kaempferol), polyphenolic compounds, and various other antioxidants (vitamins C, E) have also demonstrated strong anticancer properties.
Rosella Tomato Sauce. (Courtesy: Rosella Foods Pty Ltd)
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Carotenoids appear to be important for maintaining the integrity of gastrointestinal tract tissue. Retinoids have shown experimental gastroprotective properties – acting to prevent gastric mucosal damage from chemical exposure without adverse effects on gastric acid secretion. They can help prevent the gastric erosion associated with some drug treatments, and showed benefits for treating ulceration (stomach and duodenal). Lowered levels of carotenoids such as vitamin A and zeaxanthin have been linked to chronic gastrointestinal tract inflammatory diseases (ulcerative colitis, terminal ileitis, polyps) and gastrointestinal cancers – gastric, oesophageal, colonic and liver cancer, as well as the development of pre-cancerous lesions. Vitamin C, α-carotene and β-carotene were likewise considered to have anticarcinogenic potential against laryngeal and colorectal cancer. A deficiency of carotenoids (particularly vitamin A) has been linked to inflammatory bowel disorders such as Crohn’s disease, polyps and adenocarcinoma. Dietary carotenoids have also shown benefits for the prevention of laryngeal cancer, stomach cancer, and a reduction in oesophageal cancer risk (Rumi 1999, 2000 & 2001; De Stefani 2000a, 2000b, 2000c; Ekstrom 2000; Mozsik 2001; Levi 2000; Franceschi 2000; Tsubono 1999). It seems that the old Chinese herbalists were right after all – Tomatoes really are good for the gut. Carotenes are important for connective tissue integrity, hence the usefulness of the humble tomato (and vitamin A) in numerous eye disorders: inflammatory eye problems, optic neuritis (optic nerve inflammation), corneal ulceration and xerophthalmia (extreme corneal dryness which may be associated with vitamin A deficiency). Macular degeneration has been linked to low levels of lycopene and, although most dietary carotenoids seem to have little influence on eye health, lutein and zeaxanthin (found in broccoli and spinach) have specific potential in this condition. Thus the addition of carrot and tomato, as well as leafy green vegetables to the diet, may well protect against degenerative eye disorders and promote eyesight acuity. The supportive effects of lutein on macular pigment levels could even have benefits for hereditary eye problems such as choroideremia, a condition affecting the middle layer of the eyeball that causes progressive visual problems and blindness (Osiecki 1998; Brown 1999; Curran-Celentano 2001;
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Bernstein 2001; Olmedilla 2003; Granado 2003; Duncan 2002; Khachik 2002; Mares-Perlman 2002; Schweitzer 2002; Bone 2003; Krinsky 2003).
Medicinal ‘Peppers’
Red Bell Peppers (Capsicum annuum) have long been known to have useful dietary properties, facilitating digestion and supporting the circulatory system. The addition of this fruit to the diet may even facilitate memory, which appears to be a more unexpected benefit. Studies of mice found that a diet incorporating the peppers led to a reduction in learning impairment disorders (Suganuma 1999). (Image courtesy: Eric Hunt, GFDL, CC-by-SA 3.0)
Capsicum annuum is the source of the spice Paprika and the colourful ‘Bell Pepper’ vegetables. (Courtesy: Jo Peattie, flickr.com)
The ‘Peppers’ sourced from Capsicum annuum, C. frutescens and C. chinense contain high levels of carotenoids.6 Flavonoid constituents can vary 6 In Australia and India the name ‘capsicum’ is commonly used for bell peppers exclusively and ‘chilli’ encompasses the hotter varieties. In Britain, the sweet varieties are called red or green ‘peppers’ and the hot varieties ‘chillies’; in the USA the plants are commonly known as ‘chili peppers’ and ‘bell peppers’.
greatly according to the type of pepper, and good levels of vitamin C are present in the ripe fruit. The ripening process induces chemical changes that alter the type and amounts of carotenoids in the vegetable. It is notable that lutein and neoxanthin levels progressively decrease (and eventually disappear), while β-carotene, antheraxanthin and violaxanthin increase. Meanwhile various other carotenoids (e.g. capsorubin, capsanthin, β-cryptoxanthin, zeaxanthin, etc.) are produced. Paprika, the spice produced from dried Capsicum annuum, contains a typically diverse range of carotenoids, most of which have good bioavailability. The Red Paprika (Capsicum annuum var. lycopersiciforme rubrum) contains 34 different carotenoids (total carotenoids 1.3 g/100 g dry weight). The levels of the primary components are: capsanthin 37%, zeaxanthin 8%, cucurbitaxanthin A 7%, capsorubin 3.2% and β-carotene 9%. Other components present in good amounts include lutein and β-cryptoxanthin. Of these, capsanthin and capsorubin are uniquely found in peppers such as Paprika, albeit capsanthin is metabolised fairly rapidly in the body7 (PerezGalvez 2003; Deli 2001; Etoh 2000; HorneroMendez 2000; Oshima 1997). Capsanthin, which has potent antioxidant properties, has attracted interest for its dietary anticancer potential. Low levels (but not higher amounts) in Paprika juice have shown anticarcinogenic properties against colon tumours in animals. However, because the effect was not seen with the use of capsanthin alone, this suggested a synergistic effect with other nutritional components. Japanese studies of Capsicum annuum var. grossum (Paradicsom paprika) have supported the cancer inhibitory and chemopreventive effects of the spice (Narisawa 2000; Maoka 2001; Nishino 2002; Mori 2002). A variety of Sweet Pepper known as ‘Anastasia Red’ or ‘Anastasia Black’ (Capsicum annuum var. angulosum) has also demonstrated cytotoxic activity with selective anticancer effects that appear worthy of further investigation. Its use has 7 The bioavailability of capsanthin and capsorubin may also be relatively low in comparison with some of the other carotenoids. These compounds are also found in Asparagus, Asparagus officinalis.
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wheat. This protein (sourced from low-glycoalkaloid varieties) contains good levels of lysine and has a high nutritional value (Friedman 2006).
Ancient Potatoes
The Chilli or Cayenne Pepper (Capsicum frutescens) has become a weedy herb throughout the tropical forest due to the wide distribution of its fruit by birds. There are a couple of other species of culinary interest. Capsicum chinense is native to southern Central America, South America and western India, while the Roqueto Pepper (C. pendulum or C. baccatum) is native to Peru, Ecuador and Bolivia. Capsicum pubescens originates from the Andes and the high mountains of Central America.
even been suggested as a supplement during cancer chemotherapy (Motohashi 2003; Shirataki 2005).
Psychotic Potatoes
In any discussion of the Solanaceae the humble potato merits particular attention. The great potential benefits of dietary carotenoids have led to a reevaluation of this common vegetable. German studies of white- and yellow-fleshed potatoes (Solanum tuberosum) determined that they contained fairly significant carotenoid levels (41–131 mcg/100 g) with violaxanthin, antheraxanthin, lutein and zeaxanthin identified as the main compounds – although levels can vary dramatically (Breithaupt & Bamedi 2002). Investigations of the tubers of normal potatoes and a high-carotenoid species, Solanum phureja, showed a variation of over 20-fold (Morris 2004; Dobson 2004). Another study has given higher values for deepyellow/orange-fleshed cultivars (up to 2000 mcg/100 g fresh weight) in comparison to white-fleshed varieties (500–100 mg/100 g fw) (Brown 2005). In addition, while fresh potatoes contain only around 2 per cent protein, on a dry basis their protein value increases substantially to equal that of cereals such as rice or
Market display of potatoes, ginger and garlic.
A medley of Potato varieties. (Courtesy: Scott Bauer, USDA, Agricultural Research Service)
The wild origins of the Potato lie in the high Andean mountains where the herb flourished in the cool temperate climate. Over time the plant became subject to the influences of wild selection, which triggered the evolution of tubers characterised by great genetic diversity. This natural variation developed in response to exposure to a relatively inhospitable climate – thin poor soils, moderately long days, low temperatures and little rain. Their dietary value was recognised long ago and the potato was nurtured as an ancient crop. Tuber remains found in Peru have been dated to more than 8000 years. Ceramics with drawings of the plant have been found in burial sites from around the fourth century AD and relate to the ancient Mochica, Chima and Inca cultures. It was utilised as a food plant for even longer than this. About 200 wild tuber-bearing species of Potato (Solanum genus, Section Petota) have been identified – with the main cultivated forms belonging to Series Tuberosa (Jackson 1986).
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The Potato, which is one of the most commonly eaten vegetables in the world, is distinguished by being a relatively young food crop as far as the world market goes. Considered to be a rather unusual crop when introduced to Europe around 400 years ago, it has undergone a remarkable leap from culinary obscurity. Initially, the Potato was not entirely welcomed and did not attract serious interest until the mid-eighteenth century. The Puritans objected to it because it was not mentioned in the Bible. In Burgundy on the Continent its use was forbidden for, as John Gerard (1597) observed: ‘they were persuaded the too frequent use of them caused leprosie’. Even the famed botanist Linnaeus objected to the vegetable because of its connection with the Nightshade family. His caution, however, was understandable considering the reputation of some solanaceous herbs. There can be great toxic variability between individual Solanaceae species – as well as between the different parts of an individual plant: fruit, herb, shoots, roots or tuber. As with many others in the family, the leafy parts and green fruit of the potato are high in alkaloidal compounds with toxic potential. Over time, however, selective cultivation focused on plants with large and/or brightly coloured tubers. These cultivars were characteristically less bitter, a quality which was subsequently linked to a lower glycoalkaloid content. However, even in potatoes in the marketplace, the levels can sometimes be quite high, as indicated by this list of American cultivars (Friedman 2006): Russet potato – 100 mcg/g White potato – 43.5 mcg/g Benji potato – 98.3 mcg/g Lenape potato – 629 mcg/g. White cooking potato. The Coliban potato is a floury fleshed ‘washed’ spud that is commonly sold in Australian supermarkets – although the Sebago and King Edward are equally common. There is a remarkable diversity of others that have different culinary purposes, they include: Bintje, Desiree, Golden Delight, Kipfler, Nadine, Pink Eye (Southern Gold), Pontiac, Red Rascal and Royal Blue. Overall there are a bewildering array of potato varieties (around 4000) of which 66 are commercially grown in Australia.
Outbreaks of poisoning from potatoes have been associated with higher than normal concentrations of glycoalkaoids (α-solanine and α-chaconine) in the tubers and sprouts. While such incidents have generally involved green-skinned tubers, certain varieties can habitually contain high levels of toxic alkaloids. The Lenape potato is an example that was developed using conventional breeding methods in the 1960s that was found to have dangerously high levels of solanine in the tubers. It was quickly removed from the marketplace.8 More recently, in the 1990s, a variety known as ‘Magnum Bonum’ had to be withdrawn from the market in Sweden (NRC 2004). However, in commercially marketed potatoes solanine and chaconine are present in low levels (7 mg per 100 g or less), although toxic amounts (35 mg per 100 g) can still form in green or damaged potatoes – particularly in the ‘eyes’ and when the tuber has sprouted. The risk may not be immediately apparent because a change of skin colour does not always occur. Potatoes stored for long periods must be regarded as suspect because damage can result from exposure to both excessive light and excessive dark (Frohne & Pfander 1984; Friedman 2006). Unfortunately glycoalkaloids are heat stable, which means they can survive cooking under high temperatures. Losses in cooking are minimal: boiling (4.7% loss), microwaving (15% loss) and deep-frying (nil loss), although during frying longer cooking times at temperatures around 210° C will reduce glycoalkaloid levels. However, the cooking oil itself retains the glycoalkaloids, which can easily migrate back into the potato – accounting for a wide variability of exposure depending of whether cooking oils are regularly changed. Unpeeled potatoes will retain their toxicity no matter what type of cooking process is used because the highest alkaloid levels are located within the 1 mm from the outside surface, the content decreasing toward the centre of the tuber. The following figures show that substantial variability can exist (mcg/g): 8 This variety was based on a heritage potato developed in the United Kingdom in the nineteenth century that had lost popularity due to its susceptibility to disease. This is intriguing as breeders actually like plants with high-solanine levels in their foliage as they tend to have a higher pest and microbial resistance. Indeed, the Lenape potato is still used in conventional potato breeding programs inspiring potato varieties such as Atlantic and Denali (NRC 2004). Obviously, when the high-solanine content translocates to the tubers there can be serious problems.
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Atlantic potato – peel (83.8 mcg); flesh (36.5 mcg) Russet Nakota potato – peel (425 mcg); flesh (6.4 mcg) Dark Red Norland potato – peel (1264 mcg); flesh (22.1 mcg) Snowden potato – peel (3526 mcg); flesh (591 mcg).9 The figures for the last-named cultivar indicate that substantial amounts of glycoalkaloids can be present naturally. Under the right conditions, exposure to high levels could be quite disastrous. Therefore the potato’s skin should be removed to eliminate the chance of toxin exposure – that is, peeling and boiling is the safest form of preparation. Fortunately, there are couple of other limiting factors that reduce the likelihood of poisoning: glycoalkaloids are poorly absorbed from the gastrointestinal tract and undergo detoxification during the digestive process. The safe glycoalkaloid content in potatoes is considered to be 20–100 mg per kg (Frohne & Pfander 1984; Friedman 2006). 9 These varieties are more common in the markets of the northern hemisphere.
Glycoalkaloid Partnerships
Solanum dimorphispinum, by M Szent Ivany, Journal of the Adelaide Botanical Gardens 4, 1981. Leaf and fruit extracts of Solanum dimorphispinum (a native species) were rich in tomatine. (Courtesy: flora.sa.gov.au)
Solanum dunalianum from Papua New Guinea contains a small amount of tomatine, plus other alkaloids of interest (Bradley 1978). (Image courtesy: flora.sa.gov.au)
Solanine was first isolated from potatoes by French scientists in 1820. Another century was to pass before it was discovered that solanine was a mixture of two compounds: α-solanine and α-chaconine. These represent around 95 per cent of the total glycoalkaloids found in potatoes, although small amounts of related alkaloids (i.e. α-tomatine and solasonine) may also be present. In the potato plant the major glycoalkaloids provide natural protection against insects and other pests, tending to act synergistically to give the plant a better level of defence. More recently, calystegine alkaloids, which have a structure similar to atropine, have been discovered in potato tubers. Although their significance has not yet been determined, they also appear to be involved in plant defence and plant– insect interactions (Friedman 2006, 2004; Korpan 2004). These compounds are also found in the Physalis genus (Azemi 2006). Glycoalkaloid partnerships are characteristic of other edible fruits. The tomato glycoalkaloid tomatine was also found to be a mixture of dehydrotomatine and α-tomatine, while sola-
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margine and solasonine are the glycoalkaloid combination found in the Eggplant (Solanum melongena). Aglycones, which are the steroidal component of a glycoalkaloid, are formed during metabolic processes in the plant. Solanidine is therefore formed from the glycoalkaloids α-solanine and α-chaconine in potatoes. Tomatidine is produced from α-tomatine, and tomatidenol from dehydrotomatine (Friedman 2002, 2004). It should be noted, however, that the glycoalkaloid component of the true Tomato (Lycopersicon esculentum) is quite different to that of Australian ‘bush tomatoes’, which belong to the genus Solanum. The latter tend to contain the toxic glycoalkaloid solasodine in the unripe berries – although as they ripen they often (but not always) become edible. This is because glycoalkaloids are synthesised, sequestered and degraded at different stages of plant growth. The Potato plant, although it belongs to the Solanaceae family, does not contain nicotine or the medicinally important tropane alkaloids (hyoscyamine, scopolamine) characteristic of a number of other plants from this family. However, it does contain calystegines (nortropane alkaloids), with a greater amount in the roots, and substantially less in the growing tuber, foliage and flowers. Sprouting potato tubers have particularly high levels in the growing ‘eyes’, albeit only for a short time. These compounds have also been isolated from moths and butterflies that feed on potato plants. It is possible the calystegines have toxic attributes, which these insects appear to utilise to deter prey – although other studies have shown they have an antifeedant effect on lepidopterans (Stenzel 2006; Schimming 2005). Glycoalkaloid poisoning affects the gastrointestinal and nervous systems, as well as initiating irritating skin reactions, which can be severe with exposure to high levels.10 Sometimes it can be quite difficult to identify the culprit, as delays of 4–19 hours can 10 Potato alkaloids may be found in other genera. For instance, alkaloids from Veratrum californicum, the California False Hellebore, have pharmacological effects that resemble those associated with blighted potato poisoning (Evans 1989).
In the potato plant, glycoalkaloid production begins during germination and peaks during flowering. The leaves are the first part of the plant to gain their maximum concentration, followed by even higher amounts developing in the unripe fruits and flowers. However, the levels can differ quite markedly between cultivars (Friedman 2006).
Toxicity for the potato is not only linked to blighted or green tubers – the leaves and berries have been implicated in incidents of fatal poisoning (Friedman 2006). (Image courtesy: Dr David Midgley)
occur before symptoms manifest. Mild solanine poisoning is characterised by headache, neck discomfort, exhaustion, vomiting and abdominal pains and, possibly, fever. Gastrointestinal distress can become persistent and increase in severity, with the nausea and diarrhoea lasting up to a week. Consequently there is the risk of dehydration and the concurrent development of metabolic disorders that can lead to circulatory collapse in severe cases. Neurological disturbances range from mild distress, apathy, restlessness and visual problems, to more severe psychological problems – which can progress to paranoia, agoraphobia, hallucination and convulsions. There is potential for confusion
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in the diagnosis because the symptoms are difficult to distinguish from those of food poisoning due to Clostridium botulinum and Salmonella, which similarly disrupt nervous system function (Frohne & Pfander 1984). However, experiments have indicated that folic acid, glucose-6-phosphate and nicotine adenine dinucleotide (NAD) have protective effects against the toxicity of α-chaconine (Friedman 2004).
The Remedial Potato
Concerns about the presumed safety of some common foods has led to a re-evaluation of various Solanaceae herbs. It is possible that there are detrimental effects which may not be immediately apparent. Even minor levels of a toxin could potentially trigger a predisposition to cancer or birth defects. Some glycoalkaloids have shown teratogenic activity in animal experiments, notably the toxic alkaloid chaconine in potatoes. This has raised the possibility of a link between the ingestion of potatoes and birth
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defects – although it appears more likely that potatoes infected with the fungal potato blight would be implicated. Although unconfirmed, such effects may be related to the relatively high levels of solasodine (which is derived from solasonine) present in blighted potatoes.11 The fact that solasodine can be stored in the body’s fatty tissue for long periods may influence its toxic potential (Korpan 2004; Der Marderosian & Liberti 1988). Potatoes have had an interesting medicinal reputation – albeit little use is made of them today. They were traditionally used as an anti-arthritic, analgesic and anti-inflammatory agent. Maude Grieve (1931) commented: Successful experiments in the treatment of rheumatism and gout have in the last few years been made with preparations of raw potato juice. In cases of gout, rheumatism and lumbago the acute pain is much relieved by fomentations of the prepared juice followed by an application of liniment and ointment.12 Sprains and bruises have also been successfully treated by the Potato-juice preparations, and in cases of synovitis, rapid absorption of the fluid has resulted. Although it is not claimed that the treatment in acute gout will cure the constitutional symptoms, local treatment by this means relieves the pain more quickly than other treatment.
Remedies for rheumatism usually recommended using the hot water in which unpeeled potatoes had been boiled – although a cold infusion made from the tubers, fresh stalks and unripe berries could also be applied as a compress on painful areas. Treatments for frost-bite applied a baked potato mashed with a sweet oil to the site. Potato paste can also be utilised as an effective healing agent. A paste of peeled and uncooked potatoes has also provided a soothing emollient salve suitable for scalded or burnt skin, eye irritation, sores, and haemorrhoids – and as a cleansing cosmetic face mask13 (Grieve 1931). Extracts of potato tubers have shown antiinflammatory and antiarthritic activity in animal
This drawing from Engler & Prantl’s Die Natürlichen Pflanzenfamilien IV (1897) shows a number of the Solanaceae: A–G refer to the Potato plant, flower and fruit. Other species illustrated include Solanum lanciniatum (H); Bittersweet, S. dulcamara (J–K), S. balbisii (L), S. hystrix (M), and the Eggplant, S. melongena (N).
11 Phytoalexins are secondary metabolites that can be induced by parasitic fungi in blighted potatoes. These compounds may contribute to the adverse effects of the toxic glycoalkaloids, thereby compounding the toxicity of the damaged potato (Friedman 2006). 12 Fomentation = a hot poultice. Liniment = embrocation, a liquid for external use. 13 Leftover (boiled) potato water had another extremely practical use – it could be used to clean the silver and was reputed to restore the shine to furniture or leather goods (Grieve 1931).
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experiments (Choi & Koops 2005). So it seems there are some data that support its traditional use. Consideration must however be given to those individuals who are sensitive to (or intolerant of ) plants from the Solanaceae and find that arthritictype pain is triggered by including them in their diet. Somewhat unexpectedly, there is a report of the use of solanine for individuals suffering allergies to nightshade and cereals that gave improvement in the condition (Golubeva 1966). Solanine has also shown experimental hypoglycaemic activity (Sato 1967). In addition, the alpha forms of chaconine and tomatine have shown inhibition of the Herpes simplex virus and liver cancer cells (α-solanine was also active in the latter). Further assessments of their biological activity would be an interesting topic for future study (Thorne 1985; Lee 2004). Support for the antiviral properties of glycoalkaloids has been provided by a clinical study of an anti-Herpes cream formulation containing the glycoalkaloids solamargine and solasonine from Solanum americanum. The treatment gave excellent clinical results against Herpes genitalis, H. simplex and H. zoster, with a very high rate of non-recurrence of the lesions (Chataing 1999). The antimocrobial properties of the potato plant also appear to be diverse. Proteins with antimicrobial activity have been isolated from leaves and roots of Solanum tuberosum, and potato extracts have shown antibacterial effects against Staphylococcus aureus (Rauha 2000; Feng 2003). Various antifungal compounds have been isolated from potato extracts. Potamin-1 and AFP-J showed strong activity against Candida albicans as well as a number of other fungal species (Kim 2005; Park 2005). Chlorogenic acid, which is the main phenolic in potatoes, has antimicrobial properties and a range of other valuable activities – antioxidant, choleretic, hepatoprotective, antiinflammatory, anti-cholesterol, antiviral (anti-HIV), anti-ulcer and anti-cancer potential. Chlorogenic acid levels in potatoes decrease during dark storage, although they can be enhanced when storage conditions allow light exposure (Percival & Baird 2000). Chlorogenic acid levels also increase during episodes of greening. Unfortunately this compound is destroyed during most cooking processes, especially boiling and baking, although microwaving was found to be less destructive. Unsurprisingly, it was not present
in commercial potato products (chips, fries or potato skins) (Friedman 2006). In addition, potatoes contain flavonoids (catechin, epicatechin) – the levels of which are higher in white-fleshed varieties: 30 mcg/100 g fw, which is around twice the amount present in red- and purple-fleshed potatoes (the colour of which is derived from an anthocyanin component). Vitamin C (20 mg/100 g fw) is also present (Brown 2005). Some studies have suggested that there are other components of potatoes of medicinal interest, among them protease inhibitors of digestive enzymes (similar to those found in soybeans) that may be of value in perianal dermatitis, as well as lectins (glycoproteins) that can inhibit the growth of breast cancer cells, and chlorophylls with anticarcinogenic activity (Friedman 2006). Lectins with strong cytotoxic activity are present in potatoes. These compounds have potential as drug-delivery agents – depending on the biochemical requirements associated with different investigative, diagnostic or treatment protocols (Banchonglikitkul 2002).
Caffeic acid, which is relatively abundant in plant products, is primarily found in the form of its derivative, chlorogenic acid. This is present in substantial amounts in coffee, and is found in innumerable fruits, vegetables and medicinal plants. A cup of instant coffee contains 50–150 mg of chlorogenic acid. In raw potatoes the levels vary depending on the part of the plant examined: tuber (174 mg/kg fw), roots (263 mg), leaves (2235 mg) and sprouts (7540 mg). However, chlorogenic acid does not survive most food processing strategies to which potatoes are exposed (Friedman 2004).
CULINARY CURIOSITIES: PSYCHOTIC POTATOES AND TASTY TOMATOES
Glycoalkaloids: Poisons and Medicines
The presence of glycoalkaloids in the diet may not be all bad news. Their anticancer potential has been an interesting subject for investigation. A range of vegetable-derived glycoalkaloids have demonstrated an inhibitory effect on tumour cells (colon and liver cancer) (Friedman 2006; Lee 2004): • potatoes (α-chaconine, α-solanine, β1- and β2-chaconines, y-chaconine and the aglycon solanidine); • some potato varieties (demissidine, derived from demissine); • tomato (α-tomatine and the aglycon tomatidine); • eggplant (solamargine, solasonine and the aglycon solasodine). Alpha-tomatine, which was very active in investigations, was of particular interest – an anticancer dietary component that was around 20 times less toxic than the other glycoalkaloids. Tomatidine could also inhibit the resistance of cancer cells to drugs. Solamargine, α-chaconine14 and solanine have anticarcinogenic activity that is linked with an apoptotic activity. Studies of a number of other Solanaceae herbs (and component glycoalkaloids) have likewise suggested anticancer activity (Friedman 2006, Lee 2004): • Solanum dulcamara (solamargine and solasonine) • Solanum sodomaeum (solamargine) • Solanum nigrum (solamargine) • Solanum citrinitum and S. jabrense (solasonine) • Solanum incanum (solamargine). In addition, studies have shown that potato and tomato glycoalkaloids had a number of other interesting actions: they could inhibit the growth of the fungus Phytophthora infestans (potato blight); protect mice against Salmonella typhimurium; and potentiate the activity of malaria vaccines. Importantly, glycoalkaloids can enhance the effect of general anaesthetics that inhibit cholinesterase (Friedman 2004), although this interaction may not always be desirable. The fact that foods containing glycoalkaloids can alter the effects of anaesthesia (via inhibition of the compounds that break down the anaesthetic agents and acetylcholine) indicate that drug responses may not always be predictable (Korpan 2004). 14 Recent studies have shown that α-chaconine can inhibit cervical, lymphoma and stomach cancer cells. The compound has also shown an inhibitory effect on angiogenesis (blood supply to tumour cells) (Lu 2010).
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Tomatine from Tomatoes
Lycopersicon pimpinellifolium.
Tomatine, which is a mixture of two glycoalkaloids (α-tomatine and dehydrotomatine), was first isolated from Lycopersicon pimpinellifolium. Tomatine is dominant in green tomatoes (100x more than the ripe fruit) and lycopene is not present, with the tomatine level gradually diminishing as the fruit ripens. During ripening, tomatine forms allopregnenolone. The ratio of these compounds (dehydrotomatine: α-tomatine respectively) can change quite dramatically within the plant, increasing in the following order (mg/ kg, Friedman 2002): large immature green fruit (14:144 mg), roots (33:118 mg); small immature green fruit (54:465 mg), calyxes (62:795 mg), leaves (71:975 mg), small stems (138:896 mg), large stems (142:465 mg), flowers (190:1100 mg), senescent leaves (330:4900 mg).15 Other glycoalkaloids are also present, albeit only in very small quantities. Tomatine levels in different fruit forms or from different processing methods can be equally variable (mg/kg, Friedman 2002). • Ripe tomatoes: Sungold cherry tomato (11 mg); yellow cherry (9.7 mg); tomatillo (0.5 mg). • Unripe green tomatoes: small and immature (548 mg) or medium immature (169 mg). • Fresh processed fruit: tomato juice (28 mg); red sauce (57 mg); ketchup (28 mg); pickled green (2 samples: 28 and 72 mg). • Freeze-dried fruit: tomato juice (49 mg); red sauce (50 mg); pickled green (2 samples: 352 and 989 mg). 15 Other studies have shown that the levels of dehydrotomatine and α-tomatine were quite comparable in fresh leaves (470 & 465 mg/kg respectively), while in the brown, senescent leaves the levels could be substantially higher (6400 & 7300 mg/kg).
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Tomatoes ripening on the plant.
• Processed fruit: canned tomato sauce (57-64 mg); pickled tomatoes (114–121 mg). High tomatine-yielding fruit: • In addition, the level of tomatine in transgenic tomatoes (190–280 mg/100 g fresh weight) was increased substantially from that of the parent (35 mg/100 g) and the standard transgenic tomato (12 mg/100 g). • A high tomatine-yielding variation of Lycopersicon esculentum var. cerasiforme indigenous to Peru has been found (α-tomatine 500–5000 mg/ kg dw). This bitter-flavoured fruit, which has been relished in the local diet, is without any demonstrable acute toxic effects (Friedman 2002).
Herbarium sample of Cherry Tomato, Lycopersicon esculentum var. cerasiforme (syn. Solanum lycopersicum var. cerasiforme). (Courtesy Kim and Forest Starr, Hawaii).
The value of steroidal glycosides to a plant is based on their role in its disease resistance strategies. Tomatine has shown a diverse range of antimicrobial activity – including antibacterial, anti-yeast, antifungal and antiviral actions that not only defend the plant against microbes, but also provide defences for the developing fruit. However, the benefits that these natural substances could have against human pathogens are still a matter of conjecture (Lee 2004; Friedman 2002). Tomatine, solasonine and solamargine have all demonstrated insecticidal properties.16 Powdered, whole Tomato plants have excellent insecticidal properties and were used for this purpose in China. In particular, tomatine was shown to be very effective against red flour beetle larvae and tobacco hornworm. In Indonesia, an infusion of tomato leaf has been successfully deployed as a spray against cabbage caterpillars (Weissenberg 1998). Tomatine is lethal to snails (Lymnaea cubensis and Biomphlaria glabratus) that are the vectors responsible for diverse protozoal infections, including schistosomiasis – suggesting a possible molluscicidal role for this compound (Freidman 2002). In addition, tomato waste contains growth-promoting substances. An acid extract prepared from tomato juice waste was shown to substantially promote the growth of Cockscomb (Celosia argentea) and Tomato (Lycopersicon esculentum) seedlings. This product has potential for development as an agricultural plant growth regulator (Suzuki 2002). Tomatine has a much better safety profile than the potato glycoalkaloids. This reinforces the proposition that benefits can accrue from culinary use of high tomatinecontaining green tomatoes. The fact that tomatine has shown anti-inflammatory and immune supportive properties that could be useful in a range of inflammatory disorders and allergic reactions merits serious research consideration. In addition, the high tomatine levels in green tomatoes can have cholesterollowering effects. Tomatine binds to cholesterol and thereby facilitates its excretion (Friedman 2002). (Image courtesy: healthfoodmadeeasy.com) 16 Dried tomato leaves can yield 0.46% tomatine, which can be used as a starting point for steroid synthesis (Weissenberg 1998). A form of Tomatillo from Peru (Solanum lycopersicoides) contains levels much higher (α-tomatine 3.2–3.5% dw) than are found in the leaves of commercial tomato plants (Friedman 2002). In addition, Tomato leaves have been used as an admixture for pipe-tobacco (Weissenberg 1998).
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Insane Eggplants
The Asian origins of the Aubergine or Eggplant (Solanum melongena) are probably little appreciated by shoppers glancing at supermarket fruit and vegetable displays. The herb originated in India and has a long history as a Eggplant flower. folk remedy. Despite its widespread use in traditional medicine, the introduction of the Eggplant to European cuisine was regarded with great suspicion. Its classification in the Solanaceae ensured that it was not con-sidered safe to eat – it was even rumoured to produce immediate insanity. Of course, its purple-black skin compounded this noxious reputation during the Middle Ages, when beliefs associating darkness with witchcraft and demonic evil forces were rife. It was not until 1753 that the Swedish botanist Linnaeus accepted that the Eggplant fruit was non-toxic and listed it as edible. Even then, he bestowed upon it the provocative Latin name of Solanum insanum (later revised to S. melongena to denote its black colour). Only after Linnaeus’s ‘blessing’ did the general public accord the fruit any culinary acceptance. Throughout Asia all parts of the Aubergine plant have been used medicinally. Its natural mucilaginous soothing effects made it quite popular as a vegetable, and it was even recommended as an antidote for toxic mushroom poisoning. The plant was regarded as having laxative and astringent properties, while the leaves and rind of the fruit were recommended as an anti-dysentery remedy. In particular, the herb earned a reputation as a potent haemostatic. Carbonised (reduced to ashes), the roots, stalks and leaves had astringent and styptic properties
Aubergine fruit (Solanum melongena). (Courtesy: Zyance, GFDL, CC SA 2.5G)
which were useful for treating haematuria (blood in the urine), intestinal bleeding and uterine haemorrhage. In Malaysia the hot ash from the burnt fruit was used as a powder on haemorrhoids (Burkill 1935; Perry & Metzger 1980). Another use of the carbonised fruit was as a treatment for phlegm, ‘wind’ and digestive problems. In French Guinea the leaf infusion, which was reputed to have narcotic properties, was taken to treat a sore throat and stomach disorders. In the Philippines the roots were utilised as an anti-asthmatic remedy and general tonic (Quisumbing 1951). Chinese medicine valued the fruit as a nourishing, analgesic and anti-oedema (anti-swelling) agent. It provided a cooling remedy for fevers, and a wash prepared from the fruit decoction was used to ease the pain of chilblains. Eggplant could be made into a salve, or crushed for use as a poultice to heal hot, painful, infected and swollen sores. A remedy for tinea applied cut fruit, dipped in sulphur, directly to the infected area. In chronic rheumatism and arthritis the root decoction, or a tincture made with white wine or sake, was taken daily. A whooping cough remedy recommended a sweetened tea made from sugared fruit, while a treatment for tracheitis (inflammation of the trachea or windpipe) utilised the roots decocted with sugar. Eggplant powder (fruit and stalk roasted, carbonised and ground) was taken with warmed wine for
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and, like potatoes and tomatoes, is particularly rich in chlorogenic acid – which has substantial antioxidant actions (Shen 2005; Mans 2004; Han 2003; Barnabas 1989; Vohora 1984). Another report suggests that the use of Solanum melongena may benefit various eye disorders, notably glaucoma and convergence insufficiency (Igwe 2003). In addition, sesquiterpenoids have been recovered in fairly good quantities from root extracts of the Ethiopian Eggplant, Solanum aethiopicum (Nagaoka 2001).
Gooseberry Goodies An extract prepared from the fresh Aubergine fruit has shown significant hypotensive activity. Additionally, Eggplant fruit has been traditionally regarded as being a useful diuretic and cholagogue (bile normalising agent) (Shum & Chiu 1991). (Image courtesy: Kit O’Connell, kitoconnell.com)
use as a haemostatic to treat blood in the faeces. The dried and crushed leaf powder was similarly utilised as a tea. The whole plant has even provided an antidote for snakebite, although subsequent hospitalisation was recommended (Chang 1989). Many of these uses are supported by investigations that have shown Solanum melongena has diverse pharmacological properties – antioxidant, analgesic, anti-inflammatory and anti-allergic activities. This would certainly have influenced its efficacy in the treatment of asthma. Studies have shown that leaf extracts had a specific bronchospasmolytic (bronchial antispasmodic) activity. Additional investigations into the pharmacological properties of the leaves indicated that extracts had central nervous system depressive properties that were non-narcotic in nature and resulted in sedation (potentiated pentobarbitone narcosis) – as well as possessing an analgesic and anti-inflammatory effect. Alkaloids were responsible for the analgesic effect, while a flavonoid-based extract was anti-inflammatory. In addition, the fruit and seed were considered to have stimulant and cardiotonic properties. The Eggplant contains phenolic compounds
Weedy Physalis
Cape Gooseberries (Physalis alkekengi).
The genus Physalis, which belongs to the Solanaceae family, contains over 100 species. They are primarily weeds of cultivated areas, waste places and disturbed ground, the fruit of which have been valued as bush tucker wherever they are found. They were also widely cultivated around homesteads, which served to facilitate their spread across the entire continent. However, despite the term ‘Gooseberry,’ they should not to be confused with the true Gooseberry (Ribes sp.). The Native or Wild Gooseberry (Physalis angulata) is one of the three species most commonly encountered – and may be an ancient introduction to the
CULINARY CURIOSITIES: PSYCHOTIC POTATOES AND TASTY TOMATOES
continent. (This plant has long been confused with Physalis minima, which has a very similar distribution.) There are two other familiar species, known as ‘Cape Gooseberries’: Physalis peruviana and P. alkekengi, which were originally native to North and South America. Other weedy imports include the Tomatillo (Physalis philadelphica), Ivy-leaved Ground Cherry (P. hederifolia) and the Long-leaved Ground Cherry (P. longifolia). Today the genus is found throughout the continent, with the various species considered naturalised in different states, depending on their climatic preferences. There has been much confusion over identity. The following species distribution is currently recognised in Australia: • Physalis alkekengi: South Australia (Victoria – historical records only). • Physalis angulata (syn P. parviflora): considered to be naturalised in all states and territories except the Northern Territory, where it is regarded as a pre-European arrival. • Physalis crassifolia var. versicolor (the name P. viscosa has been misapplied to this species; P. viscosa does not occur in Australia): Queensland. • Physalis hederifolia (the names P. lanceolata and P. viscosa have been misapplied to this species): widespread in Western Australia, South Australia, New South Wales, Victoria. • Physalis ixocarpa: Queensland, New South Wales, Victoria, Lord Howe Island. lanceifolia: Western Australia, • Physalis Queensland, New South Wales, Victoria. • Physalis longifolia (syn P. virginiana): Queensland, New South Wales, Victoria. • Physalis micrantha: Queensland, New South Wales. • Physalis minima: Queensland, Northern Territory. • Physalis peruviana: widespread in all states except the Northern Territory, and occasionally found in Tasmania. Also found on Norfolk Island and Lord Howe Island. • Physalis philadelphica: Western Australia, Queensland, New South Wales. • Physalis pubescens: Western Australia, New South Wales, possibly Christmas Island (Victoria – historical records only).
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The fact that Physalis peruviana has a weedy habit and is easily cultivated led to it becoming widespread throughout the tropics. This ‘Cape Gooseberry’ was an early immigrant to Australia and the fruits have long been popular for making jams and preserves. It was originally transported by the Portuguese on their voyages between Africa and the Americas – stocked among the provisions for their long and arduous sea journeys. The herb was introduced to Australia en route to South Africa (Cape Town), where it first assumed its common name (Burkill 1935). The plant appears to have been among the earliest of the European imports to Australia, possibly arriving with the First Fleet, as the leaves were used in the early days of the colony for brewing beer (Low 1992).
Cape Gooseberry or Chinese Lantern (Physalis peruviana), which belongs to the same botanical family as the potato and tomato, yields a fruit with good keeping qualities. The golden-orange berries have a zingy tomato-like flavour. The ripe fruit, which has also been known as the Bladder or Winter Cherry, has shown antioxidant properties (LaczkoZold 2009) – as have plant extracts, which also have potent hepatoprotective properties (Chang 2008).
In India, Physalis minima has had numerous medicinal uses.17 The fruit was popular for its effective diuretic properties, which led to its use in treating dropsy (fluid retention), urinary tract disorders, gout, and gonorrhoea. These diuretic activities have been 17 It was also known as the ‘Cape Gooseberry’ – a term that has more popularly been applied to Physalis alkekengi.
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confirmed experimentally in plant extracts (excluding the roots) and are attributed to a high content of potassium nitrate (8–10%). The plant also contains steroidal lactones with a rather contradictory effect – that is, weak anti-diuretic properties (Satyavati 1987). The leaf and root of Physalis peruviana have been likewise used as a diuretic and urinary solvent (Watt & Breyer-Brandwijk 1962). The steroidal components of Physalis minima have been implicated in cases of gastrointestinal distress, but they may also be useful for steroid production. The plant’s solasodine glycoside content could be increased up to 20 times the level found in normal root samples by the use of hairy root cultures (Putalun 2004).
The Cape Gooseberry (Physalis alkekengi) can yield a prolific crop, with the potential to produce up to 300 fruit on a single plant. The attractive ripe fruit package houses a single berry encapsulated in a papery lanternlike cover. (Image courtesy: Teunspaans, Wikipedia)
Physalis alkekengi naturally grows wild in China, southern and central Europe – although it has become adopted into kitchen gardens throughout the world. While the fruit is deliciously sweet, the plant itself has poisonous potential due to its glycoside content. The herb has been employed medicinally similar to Physalis minima – as a diuretic, lithotriptic (stone dissolving), and anti-uricaemic remedy.
Physalis alkekengi, entry from the British Pharmacopoeia of 1867.
The Native Gooseberry (Physalis minima) favours a tropical habitat, particularly in Queensland, around the coast and rainforest verges.
A Herbal Panacea?
The weedy herb Physalis angulata can be found throughout the tropics. Many of its uses tend to be supported by research efforts and it has shown diverse therapeutic qualities – analgesic, anti-gonorrhoeal, anti-inflammatory, expectorant, antiseptic, antispasmodic and febrifugal actions. Other activities of interest have included anticoagulant, antibacterial, hypotensive, immunomodulatory, molluscicidal and antiparasitic properties (Taylor 1998). In addition, flower extracts of Physalis angulata have shown antioxidant and supportive effects on HDL (protective) cholesterol levels, suggesting cardiovascular system benefits (Choi & Hwang 2005). The use of Physalis angulata has been associated with a number of recommendations that suggest effective hormonal properties. It has been taken to prevent abortion (Central America), to facilitate childbirth (Fiji), treat infertility (Papua New Guinea) and as a remedy for sterility (Africa). This is of interest because Physalis minima herb (not the fruit), which has bitter properties, acts as an abortive agent in sheep The plant extract, as well as its physalin
CULINARY CURIOSITIES: PSYCHOTIC POTATOES AND TASTY TOMATOES
Physalis angulata: extracts of the plant and fruit capsules have antibacterial properties (Silva 2005). (Courtesy: Kim and Forest Starr, Hawaii)
components, notably physalins D and B (the latter is present in high levels in the leaf ) had an experimental abortifacient activity in animals. Other physalin derivatives of pharmacological interest are present in the genus, for example withaphysalin (Garcia 2006; dos Santos 2003; Taylor 1998; Satyavati 1987). Winter Cherry, Physalis alkekengi, fruit has also been utilised for fertility control in Iran. Recent studies have shown that the water-based extract contained steroidal components (3β- and 20α-hydroxysteroid dehydrogenases) with oestrogen antagonistic activity. This was suggested to result in reduced progesterone synthesis, which is normally required to maintain pregnancy (Vessal 2004). Physalis angulata has substantial antimicrobial activity that could be useful for treating drug-resistant bacterial strains. Extracts have demonstrated strong antibacterial activity against Streptococcus mutans – a cariogenic bacterium of the mouth. A mixture of physalins (physalins B, D, F, G) have shown inhibitory activity against Staphylococcus aureus, as well as Neisseria
Rhodnius prolixus – stages from nymph to adults. Physalin B from Physalis angulata can affect the blood parameters of the insect Rhodnius prolixus, an important vector for the parasitic Chagas disease (American trypanosomiasis) in South America (Castro 2009). (Image courtesy: Thierry
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gonorrhoeae. In particular, physalin B had notable inhibitory effect against Staphylococcus aureus (Hwang 2004; Silva 2005). The anti-mycobacterial properties of the genus are similarly interesting. Investigations of Physalis angulata extracts that had a broad spectrum of activity against a number of Mycobacteria strains identified physalin D as a major contributor with potential against drug-resistant strains of tuberculosis (Januario 2002; Pietro 2000). This compound was also identified as the active antimicrobial component of Physalis alkekengi extracts that were active against gram-positive bacteria – as well as possessing moderate antifungal activity (Helvaci 2010).
Essential Fatty Acids
Goldenberry (the ripe fruit of Physalis peruviana). (Image above courtesy: Flapdragon, Wikipedia)
Goldenberry (the ripe fruit of Physalis peruviana) has recently attracted interest as an excellent vitamin A resource. Overall it has a high lipid component (2–3.16%) that is rich in linoleic acid (66.4–72.42%), as well as smaller amounts of saturated acids: oleic (10–13%), stearic (2.67%) and palmitic (9.38%) – giving the oil a good polyunsaturated acid profile.18 In comparison the levels in a number of common fruits were
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much lower: Pawpaw (Carica papaya: 0.1%), Apple (Malus domestica: 0.2%), Valencia Orange (Citrus sinensis: 0.2%), Strawberry (Fragaria vesca: 0.3%) and Acerola or Barbados Cherry (Malpighia glabra: 0.2%) (Rodrigues 2009; Ramadan & Morsel 2003). Linoleic acid is an omega-6 fatty acid with anti-inflammatory and immunomodulatory properties. Oils containing it have been recommended as dietary supplements that have been successfully used for the treatment of acne, eczema, dermatitis, arthritis, premenstrual disorders, heart disease and high blood pressure. Goldenberry fruit also contains other components of interest: phytosterols (i.e. campesterol and β-sitosterol in berry and seed oil), tocopherols (vitamin E) and diverse vitamins and minerals (mg/100 g): notably iron (1.47 mg), magnesium (34.7 mg), calcium (9 mg), zinc (0.47 mg) and potassium (347 mg). Small amounts of other nutrients were also present: sodium, copper, manganese and aluminium. Tocopherols, β-carotene and vitamin K(1) were found in particularly high levels in the pulp/ peel oil (Rodrigues 2009; Ramadan & Morsel 2003). Physalis minima has been suggested as a comparable source of vitamin A, with some studies showing higher levels than P. peruviana (28.9 mg/100 g and 18.3 mg/100 g, respectively). The latter contained higher potassium and vitamin C levels, although calcium, magnesium, iron and phosphorus were comparable for the two species (Musinguzi 2007). In Egypt, studies of the juice of Physalis pubescens have shown a similar vitamin, mineral and lipid profile of nutritional interest (Sheikha 2010).
Gooseberry (Physalis minima) fruit have been similarly used to promote the healing of wounds, ulcers and abscesses, as well as being recommended as a remedy for diarrhoea (Franco 2007; Watt & Breyer-Brandwijk 1962; Perry & Metzger 1981). The leaves possess significant anti-inflammatory activity that supports these claims. The flavonoid compound, quercetin3-O-galactoside, was identified as one of the active components of the herb. In addition, extracts (whole plant) have substantial analgesic properties, albeit the antipyretic activity was shown to be insignificant (Sethuraman 1988; Khan 2009). Physalis angulata extracts have also shown potent analgesic (root and flower) and anti-inflammatory (flower extracts, withangulatin and physalin-E) activity. Some preparations even possessed good potential for drug development (Pinto 2010; Sun 2010; Bastos 2008, 2006; Vieira 2005; Choi & Hwang 2003). Recent studies of physalin F from this species have shown immunosuppressive properties that were not based on glucocorticoid (steroid) activity (Brustolim 2010). Mexican studies have shown that another species, Physalis sordida, contained a compound with a level of anti-inflammatory activity similar to that of indomethacin (Perez-Castorena 2010).
Many of the Physalis genus have been effectively used in the treatment of skin problems and wounds. A warm leaf poultice of Physalis peruviana has been considered very effective for easing inflammatory skin problems or healing skin ulceration. Extracts of the calyces demonstrated good anti-inflammatory activity, while leaf extracts had antibacterial properties. Native 18 The whole berry contains 2% oil, with the seed oil being around 90% (i.e. 1.8% of the fresh berry weight) and pulp/peel oil the remaining 10% (0.2% fresh berry weight) (Ramadan & Morsel 2003).
Physalis alkekengi, from Atlas colorié des plantes médicinales indigènes, Paul Hariot, Librairie des Sciences Naturelles, Paris, 1900.
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The use of the Native Gooseberry (Physalis minima) as an antidiarrhoeal agent is supported by investigations showing that plant extracts had antibacterial properties against gram-negative Shigella and gram-positive Bacillus cereus (Ahsan 2009). Shigella (bacterial dysentery) is associated with the development of diarrhoea (which may become bloody), fever and stomach cramps, which generally resolve within a week. Bacillus cereus and Staphylococcus aureus contamination can cause similar forms of food poisoning characterised by severe diarrhoea, vomiting and nausea.
Shigella bacteria. (Courtesy: Centres for Disease Control and Prevention Public Health Image Library, United States Department of Health & Human Services)
Table 4.1 Traditional uses of medicinal plants of the Physalis genus Species and medicinal properties Physalis alkekengi Chinese Lantern Medicinal properties: Diuretic Antitussive Expectorant Febrifuge Anti-inflammatory Physalis angulata Medicinal properties: anti-inflammatory antiseptic and antibacterial; anti-asthmatic; liver protective; anti-diabetic; diuretic; vermifuge; analgesic
Medicinal reputation (reference) Chinese medicine (Duke & Ayensu 1985): • Combination remedy: flower used with Arctium, Liquorice (Glycyrrhiza, Gan Cao), Scrophularia for treatment of respiratory disorders (bronchitis, coughing, sore throat) including whooping cough. • Fruit: diuretic; used to treat gout, jaundice, rheumatism • Plant: treatment for diabetes, dysentery, respiratory problems (bronchitis, pertussis, pharyngitis, sore throat, tonsillitis, tracheitis), jaundice, and gas pains (intestinal). Used also to treat boils and abscesses and pemphigus (a rare and painful blistering autoimmune skin disease).
Weiner (1985): • Fiji: liquid pressed from leaves given to facilitate childbirth. • Tonga: leaves used medicinally. • New Guinea: seeds used in treatment for female infertility. Papua New Guinea (Holdsworth 1993; 1989): Juice squeezed from fire-heated leaves and applied to cuts and scratches; leaves squeezed into water and solution drunk as abortifacient (taken daily if necessary). Colombia (Taylor 1998): • Fruits and leaves said to have narcotic properties. • Decoction used as anti-inflammatory and disinfectant: asthma, skin diseases. Brazil (Taylor 1998): • Herb: anti-inflammatory and antiseptic for skin disorders, and the plant sap used for treating earache. • Sedative, diuretic. • Kidney, liver and gallbladder problems (hepatitis, jaundice), chronic rheumatism, fever, vomiting.:
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Peru (Taylor 1998) • Leaf/plant infusion: anti-inflammatory, diuretic, rheumatism, worms, earache, malaria, asthma. • Liver disorders: roots for hepatitis. • Antidiabetic remedy: macerate the roots of three plants in rum (250 ml) for a week, and then add honey. The dose was 1/2 glass taken twice daily for 2 months. Note: The calyces of the Mexican Husk Tomato (Physalis ixocarpa syn. P. aequata) were likewise made into a decoction as an anti-diabetic remedy in Mexico (Morton 1986). Physalis heterophylla Medicinal properties: wound healing; antibacterial; emetic Physalis lanceolata Medicinal properties: analgesic; wound healing; gastrointestinal disorders Physalis minima Native Gooseberry, Cape Gooseberry, Lesser Ground Cherry Medicinal properties: antibacterial; antidotal; alterative; diuretic; tonic
American Indian (Moerman 1986; Foster & Duke 2000): • Infusion of dried leaves and roots: wash for scalds and burns; used as emetic to treat bad stomach-ache; wash for venereal disease. • Seeds: urinary disorders (difficult urination), fevers, inflammation.
American Indian (Moerman 1986): • Root decoction: headache, stomach trouble. • Root: dressing for wounds. • Root in smoke treatment: medicinal.
Indian medicine (Satyavati 1986; Chopra 1956): • Leaves: mixed with water and mustard oil are used in earache and deafness. • Fruits: reported tonic, diuretic, aperient, used in gonorrhoea; also reported useful in snake bite and scorpion sting; fruit forms an ingredient of oily preparation used in splenic disorders. Indian medicine (Watt & Breyer-Brandwijk 1962): • Fruit: alterative (general cleansing), aperient, diuretic, purgative properties; used to treat dropsy, urinary disorders and gout. • Fruit: popular tonic that was reputed to infuse vigour ‘in a worn out system and to offset premature decay’. • Konkan (India): plant paste with rice water applied to flaccid breasts. • Vietnam: plant used as diuretic. Malaysia (Burkill 1935): • Herb: poultice for headache and intestinal pain. • Fruit: poultice was applied locally to treat headaches and intestinal pains. • Leaves smeared with oil heated and applied to ulcers; poulticed on wounds and pustules. • Leaf decoction with Plantago major for gonorrhoea; has a diuretic effect. • In Java used the root was used as a vermifuge (for worm removal) and febrifuge (to treat fevers). Malaysia (Ahmad & Holdsworth 1995): Root decoction of Physalis minima was taken to treat hypertension and diabetes.
Physalis peruviana Cape Gooseberry Medicinal properties: gastrointestinal disorders; anthelmintic; diuretic; anti-asthmatic; anti-inflammatory Physalis pubescens Downy Ground Cherry
Africa (Watt & Breyer-Brandwijk 1962): • The Zulu used a leaf infusion as an enema for abdominal upsets in children. • Europeans applied heated leaf poultice locally to draw out inflammation. India (Morton 1986): The leaf juice was given for worms and bowel problems. Colombia (Morton 1986): Leaf decoction taken as a diuretic and anti-asthmatic remedy. Duke & Ayensu (1985) • Chinese medicine: plant: decoction to treat abscess, carbuncles, fever, pemphigus, sore throat, worms. • Venezuela: cholera. • Haiti: colic, dropsy, fever, nephritis. • Yucatan: earache. • Puerto Rico: stomach ache, toothache. • West Indies: tumours of the testicles.
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A Medicinal Future
The Physalis genus appears to have useful antiparasitic attributes – with investigations focusing on the antileishmanial, antimalarial or trypanocidal activity of these plants. Extracts of Physalis angulata had interesting antiplasmodial activity against the malaria parasite, and clinical studies of an antimalarial herbal treatment that included this plant gave good results19 (Lusakibanza 2010; Ankrah 2003). The plant also possessed anti-trypanosomal activity that appeared to be associated with its withanolide components (Vieira 2008; Abe 2006; Nagafuji 2004). Physalins (notably physalins B and F) have been identified as the active components against the leishmaniasis parasite, some of which have shown potent leishmanicidal activity20 (Guimarães 2009; Atta-ur-Rahman 2008; Choudhary 2007 & 2005). Physalis angulata extracts (whole plant, roots, and physalin constituents) have also shown molluscicidal activity against the snail vectors that transmit some of these parasitic disorders (dos Santos 2003). Investigations have also lent support to the use of various Physalis species in folk medicine traditions for the treatment of inflammatory conditions (e.g. arthritis), cancer, leukemia and hepatitis. Evaluations of the antiviral (anti-HIV, anti-poliovirus), antimutagenic, anticancer (apoptosis-inducing) and cytotoxic attributes of various species have shown interesting results: • Physalis angulata: Flavonol glycosides were among the compounds in that were identified as having ‘remarkable cytotoxicity.’ The herb contains a range of physalins and withanolides21 with antitumour properties, as well as β-sitosterol and chlorogenic acid (Lee 2009; Lee 2008; Damu 2007; He 2007; Magalhães 2006; Hsieh 2006; Ismail & Alam 2001; Taylor 1998).
19 The study was undertaken at the Noguchi Memorial Institute for Medical Research, Legon, Ghana and the formulation was called AM-1. In addition to Physalis angulata, the other ingredients were Jatropha curcas, Gossypium hirsutum and Delonix regia (Ankrah 2003) 20 Physalins for these studies were extracted from P. angulata and P. minima. 21 The anticancer compound withaferin A is present in Physalis virginiana, and in the Costa Rican anticancer herb Acnistus arborescens. Physalin D (from Physalis minima) has also shown experimental anti-tumour activity (Duke & Ayensu 1985).
Withanolides
Indian Gooseberry, Withania somnifera, is an important withanolide-containing herb that has been highly valued as a tonic in Ayurvedic medicine. (Courtesy: Ashishbhatnagar72 Wikipedia)
Withanolides are important chemical components that have been found in diverse Solanaceae species. Around 300 different withanolides, which are naturally derived from steroids, have been discovered. Even though the practical pharmacological value of the majority has yet to be determined, many have been investigated for their insecticidal and pesticidal properties. Withanolides have attracted a great deal of interest for their antimicrobial, antineoplastic, immunosuppressive, anti-inflammatory and antiarthritic properties. These components are likely to influence the therapeutic value of Solanaceae medicinal plants such as the Cape Gooseberry (Physalis peruviana), Physalis minima, Indian Ginseng (Withania somnifera), Henbane seeds (Hyoscyamus niger) and some Datura species (e.g. D. fastuosa). They also illustrate some close chemical relationships between different genera. For instance, closely related compounds named acnistins and dunawithanines have been isolated from the Dunalia genus, which also belongs to the Solanaceae. Acnistins have shown immunosuppressive properties – as have withanolides from Withania somnifera (Veras 2004; Moreno-Murillo 2001; Lischewski 1992; Luis 1994; Sudhir 1986; Satyavati 1987).
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• P hysalins B, F, G and H from P. angulata have demonstrated immunosuppressive properties that could be useful therapeutically – for example, in the suppression of transplant rejection (Yu 2010; Soares 2006 & 2003). • Physalis minima: utilised as an anticancer remedy in Malaysia and Thailand and has shown experimental activity against lung adenocarcinoma, breast and ovarian cancer cells. Extracts had high activity and excellent clinical potential. Physalins were identified among the active cytotoxic agents (Ooi 2010a, 2010b; Leong 2009; Lee & Houghton 2005). • The Tomatillo (Physalis philadelphica): contains withanolides with cytotoxic properties. Of these ixocarpalactone A was of particular interest as a cancer chemopreventive agent (Choi 2006). This species is widely used in Mexican cuisine. • Physalis peruviana: Investigations of leaf and stem extracts showed good activity against colorectal and prostate cancer cells, as well as chronic myeloid leukemia and anti-hepatoma (liver cell cancer) properties. The withanolide 4β-hydroxywithanolide E from Physalis peruviana was of particular interest in lung cancer studies (Martínez 2010; Yen 2010; Quispe-Mauricio 2009; Wu 2009, 2006, 2005, 2004a, 2004b; Arun & Asha 2007).
Studies of Physalis peruviana have indicated substantial anticancer (apoptosis-inducing), anti-inflammatory, anti-oxidant and hepatoprotective activity. In addition, the use of Physalis peruviana fruit juice for treating pterygium of the eye has been reported in Colombian traditional medicine. Evaluation of the anti-inflammatory and cytostatic activities of the remedy determined that it acted to inhibit fibroblast growth and thereby had an anti-pterygium effect (Pardo 2008).
The Shoo-fly Plant, Apple of Peru
Nicandra physaloides, the Shoo-fly Plant.
The Shoo-fly Plant, Nicandra physaloides, which is closely allied to Physalis, produces fruits with toxic potential that appears to be mild although the seeds contain a poisonous principle named solanin. Like many other plants in the Solanaceae its toxicity is probably related to the ripeness of the fruit. Few medicinal properties appear to be attributed to the herb, although in Madagascar the leaves were used as a cure for asthma and skin diseases. They were also used in a decoction for treating dandruff. The Shoo-fly Plant is a decorative ornamental of Peruvian origin that became widespread in cultivation for its Chinese lantern-like fruits. It has become equally widespread as a weed throughout the tropics. Its proliferation becomes troublesome around summertime when it contaminates farm crops (especially maize), and invades the rainforest edges or cleared areas such as road verges. In the more southerly regions (New South Wales, Victoria) its growth is not as vigorous due to the cooler climate (Lamp & Collett 1996). The common name ‘Shoo-fly’ was derived from the plant’s reputation for fly-repellent and insecticidal properties. It was said to be particularly effective for killing whitefly. Withanolides from this plant have insecticidal activity (Moreno-Murillo 2001).
•
CULINARY CURIOSITIES: PSYCHOTIC POTATOES AND TASTY TOMATOES
The diversity of Solanaceae that can be utilised as fruit and vegetables provide an interesting insight into the complexities of plant chemistry and, as with the Convolvulaceae, there is a long association with cultivation in agriculture to produce less toxic crop varieties. A number of other plants have undergone similar selection processes, albeit for different toxicological reasons. These include a diverse array of oxalate-containing vegetables that include the wellknown Taro root of the Pacific, Asia and Africa – and some common greens such as spinach, beetroot and chard. The irritant effects of oxalates are often neutralised by basic detoxification processes, although
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this is not always the case. There are some plants that are simply inedible and unusable no matter what processing they are subjected to – a couple were even deliberately utilised inhumanely as a means of coercion and punishment during the era of the slave trade. Aroids, in particular, are known for their irritant effects, so it is surprising to find that they have an extensive economic role – and not only as food products. There is a massive market in their propagation as ornamentals – although their propensity to become invasive weeds (which is often ignored) is surely to their great detriment.
Weedy aroids in the rainforest canopy, and smothering a native palm.
Chapter 5
AROIDS: IRRITANT POISONS
The Aroid or Arum lily family (Araceae) contains around 2000 different species worldwide. Aroids are a common feature of tropical and subtropical gardens across Australia – often taking a spot as a prized ornamental although, just as often, they make their presence felt as a weed. The most common are the Arum and Calla Lilies (Zantedeschia spp.), Peace Lilies (Spathiphyllum spp.), Dumbcane (Dieffenbachia spp.), Philodendrons (Philodendron spp.) and the SwissCheese Plant (Monstera deliciosa). Encounters with Aroids have been recorded from the earliest days of exploration. Records readily attest to large areas of Cunjevoi, Alocasia macrorrhizos (known in the Pacific Islands as Giant Taro) in northern Queensland and its use as a vegetable. In 1873, G Elphinstone Dalrymple, while surveying the Johnstone River region, made the following observations with regard to its harvest at an Aboriginal camp: ‘a dilly basket full of human bones and skulls1, and several packages of stuff tied up in banana leaves, and having the appearance of pounded potatoes, probably made by the gins from the Tara [sic] which covers hundreds of acres in strips along the river banks, the leaf being exactly similar to some from the South Seas in the Brisbane Botanical Gardens. These Tara beds were here and there grubbed up over considerable patches by the blacks.’ In 1770 both Joseph Banks and Captain James Cook experimented with the root as a foodstuff at the Endeavour River encampment – which is now the township of Cooktown. The wild corms that were collected, which were small and not particularly appealing, required a lot of processing before use. Ornamental forms of Alocasia macrorrhizos at the Flecker Botanic Gardens, Cairns. All have a reputation for toxicity.
1 Bones and skulls lying around may sound somewhat unusual, but some Aboriginal people carried their dead with them for a period of mourning before their final burial rites.
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Banks wrote: ‘Some of the Gentlemen who had been out in the wood Yesterday brought home the leaves of the plant which I took to be Arum Esculentum, the same I believe as is calld Coccos in the West Indies [i.e. Colocasia esculenta]. In consequence of this I went to the place and found plenty; on tryal however the roots were found to be too acrid to eat, the leaves however when boild were little inferior to spinage’. Banks mentioned that more laborious preparation strategies were utilised by their companion: ‘Tupia by Roasting his Coccos very much in his oven made them lose intirely their acridity; The Roots were so small that we did not think them at all an object for the ship so resolvd to content ourselves with the greens which are calld in the West Indies Indian Kale.’ Despite all the preparation, Cook’s comment after trying them probably best summed up their popularity: ‘the roots were so bad that few besides myself could eat them’. Obviously they were not going to rate as a delicacy for future explorers.
Australia. Cunjevoi, Alocasia macrorrhizos, is the native Australian species. Taro, Colocasia esculenta, appears to have been introduced to this continent long ago by early visitors. Indeed, it has been present in the rainforests of northern Queensland for at least 10,000 years (Haberle 2005). Wild populations can also be found distributed from Western Australia (east Kimberley), to the Northern Territory (Arnhem Land). Taro’s widespread cultivation has meant that it has become naturalised along much of the east coast of Australia. Today, the plant can be found as far south as Sydney, with imported varieties sometimes found as wild garden escapees (Low 1992).
The Difference Between Taro and Cunjevoi Cunjevoi (Alocasia macrorrhizos) and Taro (Colocasia spp.) are easily confused as they have a very similar appearance, with differences that are more truly apparent to the botanist than the lay person. Both favour river banks and creeks, where there is plenty of water and sun exposure in contrast to the deep gloom of the adjacent jungle. The leaves are also very similar although there are differences in the plants’ appearance. Cunjevoi produces an impressive spike of arrow-shaped leaves that generally grow from ground level, albeit older specimens may develop a short trunk. The
Taro in riverine habitat.
Purple-stemmed Taro.
Taro is thought to be originally native to India, although it has been cultivated throughout Southeast Asia since antiquity. Taro and Cunjevoi share a similar habitat and distribution – ranging from India, Southeast Asia and the Pacific Islands to
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Giant Alocasia: note arrow-shaped leaves and stem insertion at leaf base.
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Cunjevoi leaf stalk is inserted into the edge of the leaf and the inedible fruit is red. Taro, which tends to be a smaller plant, has the leaf stalk attached at the back of the leaf (around a third of the way up) and produces green berries (Hiddins 2001; Low 1992).
A Continuing Botanical Conundrum?
Taro tubers. (Courtesy: Kim and Forest Starr, Hawaii)
Cunjevoi: cultivar.
Red fruiting spike of the ornamental Cunjevoi.
Ornamental Taro planting.
The flowers of Cunjevoi (Alocasia macrorrhizos, syn. A. macrorrhiza in much of the older literature) and Taro (Colocasia esculenta) are typical of the Aroid family, with a large green bract covering a pencil-shaped flower spike, the male flowers above and the female below. They appear in early summer. The flowers have a heavy, sweet scent and are particularly attractive to native bees. Taro flowers are edible and have been utilised in meat dishes and stews. They are, however, not particularly common in cultivated crops and rarely set seed (Abbott 1982).
The Taro, Colocasia esculenta, is possibly the most familiar of the large-leaved ornamental Aroids that can be utilised as food. The plant was first described by Linnaeus in 1753 as two distinct species – Arum colocasia and A. esculentum. The genus was revised in 1832 by Schott, and the names changed to Colocasia antiquorum and C. esculentum respectively – with the name Arum being reserved for other species that had been previously placed in this genus. However, in 1856 Schott changed his mind and reclassified them as the single species Colocasia antiquorum, and the other Colocasia species were considered to be varieties. This convention held for around 80 years until 1939, when Hill reviewed the genus. He felt the name Colocasia esculenta took precedence over C. antiquorum, in accordance with the first names used by Linnaeus (Arum colocasia and A. esculentum). Even so, this does not seem to have resolved the issue. Debate continues as to
AROIDS: IRRITANT POISONS
whether there are two species (C. esculenta and C. antiquorum), or one with many varieties. Some have resolved the problem by considering C. esculenta as the major species, with two varieties: C. esculenta var. esculenta, and C. esculenta var. antiquorum (Gomez-Beloz & Rivero 2006). Today around 20–25 species of Colocasia are recognised.
Ornamental forms of Taro (such as this Black Taro, Colocasia esculenta fonatinesii) and Cunjevoi that vary in colour from dark green to purple can be found as garden escapees in the urban landscape. Those that are almost black in appearance have been particularly prized.
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Hazardous Encounters with Native Aroids
Wild Taro gained a somewhat dubious reputation throughout its entire range due to its well-recognised toxic properties. Since ancient times the plant has been subjected to a painstaking detoxification process that is essential to remove the acrid juice and break down its irritant calcium oxalate content. Early Australian medical practitioners quickly became familiar with its hazardous nature. Dr John MacPherson issued an eloquent warning to this effect in the Medical Journal of Australia in 1929: When fresh, the corm is considered to be a deadly poison. The stout stem also contains this acrid principle. The leaves and petiole are likewise full of the burning juice which will blister the lips if applied to them. Taken internally by man or beast, it causes great pain and swelling in the throat and tongue and is an intense gastric irritant. Curiously enough, I noticed a tame native magpie of mine picking and eating portions of the young leaves without suffering any evident ill effect. I observed also that on my own unbroken skin of the hand the sap of the young leaf had no irritant actions. Prolonged contact, however, of the juice of the mature leaf may cause vesication and pustulation. A newspaper account mentioned that some years ago a 4 year old girl who had chewed some cunjevoi flowers, died ‘raving mad’ 6 hours afterwards. If unwashed hands, after touching the flowers, come in contact with the eyes the juice of the corm or leaf may cause intense conjunctivitis or destructive inflammation of the eye and may permanently impair or destroy vision. It has been stated that the juice was used by the blacks to poison their spear heads. It does not, however, appear adapted for that purpose.
Australian Brush TurkJ186 ey (Alectura lathami). Surprisingly, some native wildlife can find Taro roots palatable. The botanist RH Cambage commented on the Brush Turkey’s harvest of Colocasia macrorrhiza (possibly Alocasia brisbanensis) at Mount Bellenden Ker in northern Queensland: ‘Some of these plants were noticed to be prostrate, and it was pointed out by the natives that the roots are eaten by the Bush Turkeys (Talegallus Lathami) [sic] which undermine the plants when scratching for their food. This is evidently the plant referred to by Professor Baldwin Spencer as being eaten by the Native Turkeys near Cooran, south of Gympie’ (Cambage 1915).
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Detoxifying Tubers for Food and Medicine
Alocasia brisbanensis was formerly considered to be a variety of Cunjevoi, A. macrorrhiza var. brisbanensis. This species is found not only in the Brisbane region, but extends its distribution into northern New South Wales. The plant has also been found in northern Queensland.
FM Bailey mentioned the culinary and medicinal use of Cunjevoi in the Journal of the Royal Society of Queensland (1884): ‘Colocasia macrorrhiza: This plant is the “Pitchu” of the Burnett aboriginals, the rhizome, partially dried and roasted in the ashes, are eaten by them as food. The leaves are frequently used with good effect by European settlers as a vesicatory in cases of acute rheumatism.’ The preparation of the rootstock was a laborious undertaking. Pastoralist Tom Petrie provided details in his memoirs of early Queensland (1837): ‘A large leaved plant, which grew on the edge of the scrubs (Alocasia macrorrhiza), was also sought for its roots. It is well known as “cunjevoi”, but the Brisbane blacks called it “bundal”. This plant is poisonous, but the blacks prepared the roots by soaking them a long time, and then they were pounded up and made into cakes, and so roasted on the cinders.’ The resultant dough was described by Dr MacPherson as an ‘insipid, farinaceous mass’ that ultimately resulted in a spicy tasting grey-green cake: ‘The alternate roastings and poundings were persisted in for a day or two, when it was ready for use. Sometimes it was first well washed. It does not make a tempting looking viand, resembling black and yellow clay more than anything else’ (MacPherson 1929).
In northern Queensland the root was treated similarly: ‘This is the ordinary method of preparation at Cooktown, on the Bloomfield and the Tully Rivers. At Atherton, and sometimes at Cooktown, after the roots have been roasted, they are placed on a specially constructed grid framework about 15 or 18 inches above the fire. Here they are left for some considerable time before being ultimately pounded’ (Roth 1901). In the Northern Territory, at Groote Eylandt, the roots were thrown into the fire to roast before being eaten. However, the job of detoxifying them was such a labour-intensive operation that it generally fell into disuse once alternative foods became available. Dr MacPherson mentioned some other native Arum lilies that were utilised in a similar manner to Taro and Cunjevoi – certainly the processing was equally laborious: ‘In addition, two species of Typhonium indigenous to Australia may be mentioned that are members of the Arum family. Typhonium brownii inhabits NSW and Queensland. It also has acrid properties. The native blacks remove the acrid principle of the rhizome or tuber by a process of pounding or roasting, when it forms an article of their diet. Typhonium angustifolium is the “wanjallo” of the Queensland aborigines. The bulb or tuber is roasted, broken with a stone, pounded a great deal and again roasted several times before being eaten as food’ (MacPherson 1929). Walter Roth recorded of Typhonium brownii tubers: ‘If raw they produce a burning sensation like a chili. They are roasted for a minute or two in the ashes, then pounded between two stones, roasted again and pounded, and so alternately for a good 10 minutes or more until they come out finally of the consistency of a piece of India rubber’ (Roth 1901). The description does not sound the least bit appetising. Cultural historian and ethnobotanist Jennifer Isaacs commented that, Cunjevoi roots are extremely poisonous and must be thoroughly processed before being considered edible.
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even after all this preparation, the tuber could cause a headache if too much was eaten. She noted that the red-flowering Western Australian species, Typhonium liliifolium, was utilised similarly in the Kimberley region for making a sausage-like foodstuff that had good keeping qualities (Isaacs 1994). In the Northern Territory Typhonium alismifolium and T. flagelliforme were likewise considered edible after being crushed and roasted (Lindsay 2001; Yunupinu 1995; Wightman & Smith 1989).
Native Typhoniums
Typhonium brownii. (Courtesy: KAW Williams, Native Plants of Queensland, Vol. 1)
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There are nineteen species in Australia, the majority of which are endemic, including a couple from the Northern Territory that remain unclassified. These plants are widespread throughout the northern part of the continent. Only one species (Typhonium alismifolium) ranges to South Australia, while two are found in New South Wales (T. brownii and T. eliosurum). The tubers were once widely utilised by Aboriginal people for food – for instance, Typhonium angustilobum produces a circular flattened tuber that is crushed and roasted before use. This species is known as the Duck’s-foot Yam due to the shape of the leaf. The various native species may well have had medicinal uses, although there does not appear to be any records of this. Certainly Typhonium blumei (which is naturalised) and the native species T. flagelliforme have been used medicinally in Asia. The latter has recently attracted a lot of attention as an anticancer cure.
Medicinal Typhonium tubers
Bai Fu Zi, the tuber of Typhonium giganteum, prepared for use in Chinese herbal medicine. Typhonium brownii.
Typhonium is a small genus of Araceae herbs that ranges from India and China to Indonesia, Japan and northern Australia.
Historically Typhonium giganteum has been employed in Chinese medicine to relieve pain, remove toxic materials from the body, and promote vital energy circulation. It also possesses expectorant properties for the treatment of respiratory disorders. Its reputation as
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a resolvent and detoxicant remedy for growths (lumps and hardenings) has suggested its use for the treatment of lymphatic congestion and tumours (Chang 1992; Yeung 1985). Of particular interest is its deployment for a condition called ‘wind-phlegm’, associated with spasms, seizures or convulsions. This corresponds with the concept of cerebrovascular accidents (stroke) and epilepsy in Western medicine (Chang 1992; Yeung 1985). Studies have isolated cerebrosides from the remedy (tuber), with antispasmodic potential (Gao 2007). An analgesic activity of Typhonium giganteum (rhizome extracts) has been confirmed experimentally (Sampson 2000). The closely related species Typhonium flagelliforme, which is native to Queensland and the Northern Territory, has also been utilised for respiratory disorders (possessing cough-relief, expectorant and anti-asthmatic activity), and as an analgesic, anti-inflammatory and sedative agent (Zhong 2001). In addition, a cerebroside with significant anti-hepatotoxic activity has been isolated from this species (Huang 2004). In Malaysia, where it is known as the ‘rodent tuber’, Typhonium flagelliforme gained a measure of fame as an anticancer remedy. The plant (leaves and tuber) has been used for treating leukaemia, breast and cervical cancer. While it rated poorly in the cytotoxic
cell studies that are initially utilised as an indication of anticancer potential, later investigations observed antiproliferative and apoptosis-inducing effects in cancer cells. Recent studies have indicated extracts had particularly good anti-leukaemic potential, and pheophorbide components were among those isolated from the active anticancer fraction (Lai 2010, 2008; Mohan 2010a, 2010b, 2008b; Nobakht 2010; Choo 2001). Clinical reports support the effective use of the remedy in cervical cancer, showing excellent results (www.j-medicalinfo.com/treating-cervical-cancer. html). Additional investigations of Typhonium divaricatum have isolated a lectin from tuber extracts with antiproliferative and antiviral activity that has potential for use in investigative chemical studies for cancer and HIV (Luo 2007). In addition, studies of Typhonium trilobatum, an Indian species, indicated that tuber extracts had excellent antibacterial activity, suggesting it could be a useful candidate for treating drug-resistant bacteria such as Staphylococcus aureus and Pseudomonas aeruginosa (Kandhasamy & Arunachalam 2008). Typhonium flagelliforme (hexane extract) has shown equally interesting antibacterial potential against the gram-negative bacteria Pseudomonas aeruginosa and Salmonella choleraesuis – as well as good antioxidant activity (Mohan 2008a).
Table 5.1 Summary of the traditional medicinal uses of Typhonium species Species and main indications Typhonium blumei*
Typhonium divaricatum* Wound healing; respiratory disorders
Typhonium flagelliforme* Anticancer; anti-inflammatory; anti-asthmatic; detoxicant
Medicinal reputation India, Southeast Asia (Kandhasamy & Arunachalam 2008): • Tuber: poisonous. • Use: traumatic injury, snake bite, abscess, lymphotuberculosis (tuberculosis of the neck lymphatics, i.e. scrofula) and ‘vacuities’. Duke & Ayensu (1985): • Leaf extract: used in Chinese medicine for treating internal injuries (very small doses are used to avoid toxic reactions – i.e. numbness, vomiting). The leaf (boiled) was applied to bruises. • Flower (inflorescence): reputed to have healing, resolvent and styptic attributes. • Tuber: employed as an expectorant for respiratory disorders (including cough) and as a rubefacient. India, Southeast Asia (Kandhasamy & Arunachalam 2008): • Respiratory disorders: cough, to reduce phlegm (expectorant). • External use: traumatic injury, abscess. Malaysia (Zhong 2001): • Popular use as anticancer remedy; antileukaemic potential. • Medicinal use: respiratory problems, anti-asthmatic, sedative, analgesic. • Experimental studies support its use in respiratory disorders, particularly cough and asthma.
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Southeast Asia, India, Sri Lanka (Mohan 2008a, 2008b): • Leaves wrapped in Longan flesh and eaten. • Fresh juice extracted from the whole plant has been mixed with honey and taken as a drink. Karuppiah (1999): Studies have supported an anticancer effect: juice extract has shown anticancer activity in hepatic (liver) cells. Choo (2001): Extract had low cytotoxicity; the juice extract contains a high concentration of the amino acid arginine (0.874%), as well as a high tryptophan content (0.800%). Typhonium giganteum Anticancer; antispasmodic; analgesic; carminative; detoxicant; expectorant
Yeung (1985); Duke & Ayensu (1985): • Tuber (root): antispasmodic in ‘wind-phlegm’ conditions: dizziness, seizures, convulsions, numbness, paralysis, headache. • Useful for treating painful conditions such as rheumatic pain, migraine and tetanus. • Respiratory disorders: anti-asthmatic, cough with profuse phlegm. • Employed as a cure for gastralgia and arthralgia due to ‘blood disorder’ and for treating snake bite. • Disperse lumps and ‘hardenings’: antitumour, scrofula, lymphatic congestion. Perry & Metzger (1981): Typhonium rhizome is scraped with bamboo to remove the outer skin, sliced and then soaked in water with pieces of ginger before being dried for storage; properties are biting, hot, slightly poisonous warming; used for stroke, tetanus, localised headache
Typhonium hunanense Detoxicant Typhonium trilobatum* Antibacterial
Chinese medicine (Chang 1992): ** • Tuber: employed as a cure for lymphotuberculosis (tuberculosis of the lymph glands, usually associated with swelling of the neck). • A treatment for scrofula used a local application of fresh lotus root pounded with a little egg white and applied to the lesion. Similar external applications were employed to treat reticulocytic sarcoma (a form of cancer affecting reticulocytes, i.e. immature red blood cells) and lymphoma (tumour of the lymphatic system) – the ‘fresh lotus’ or the powdered herb made into a paste. India (Kandhasamy & Arunachalam 2008): Use: swelling, snakebite, abscess. India (Kandhasamy & Arunachalam 2008): Useful for treating skin eruptions; piles (haemorrhoids), traumatic injury, lymphatic tuberculosis, tetanus India (Chopra 1956): • Tuber eaten with bananas as a stomach ache cure. • Root: stimulant; applied externally to bites of venomous snakes and at same time taken internally. Perry & Metzger (1981): • Acrid tubers: used in poultices as counter irritant (Burma). • Heated leaves: poulticed on boils (Burma). Prepared tuber pulp (ground with adas-poelasari, Foeniculum vulgare, seeds, and • thinned with vinegar) applied to skin eruptions (Indonesia).
* These four species, as well as T. roxburghii, have been confused in the literature. T. blumei and T. flagelliforme have been erroneously listed as T. divaricatum. The names are given here as per author citation. ** Aconitum coreanum has also been used as Rhizoma Typhonii – although Chang (1992) comments that the two drugs have very different actions and should not be employed as substitutes. Aconite species contain aconitines, which are highly toxic, albeit Chinese medicine utilises a number of effective detoxification strategies (Chang 1992). However, in some regions of China Typhonium giganteum is regarded as having a better effect than Aconitum, which has probably led to a measure of confusion between the two (Perry & Metzger 1981).
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Lectins for Biochemical Investigations
Aroids contain an extremely interesting class of compounds known as lectins, widely used in investigative biochemistry as they have specific binding actions with polysaccharides or glycoproteins. Importantly, the reaction is reversible and does not induce chemical modifications of the target cell. For this reason they have attracted great interest for use in biochemical studies – with different lectins acting on different target cells, which can make them suitable for use in specific investigations. Lectins can detect subtle differences in complex carbohydrate structures and can selectively bind to different bacteria, yeasts, viruses, protozoa, plant and animal cells. Lectins have been considered good candidates for cancer research as they can detect alterations in malignant cells and, in some instances, have the ability to reduce cellular tumorigenicity. Many lectins have antiviral properties that are suitable for the study of HIV infection cycles and chemotherapy responses. Lectins can also be useful for determining a patient’s immune status. Aroid lectins have been of particular interest for their specific ability to bind to glycans or glycoproteins, yet they have only a weak affinity (or none) for oligosaccharides. This type of lectin has been isolated from Dumbcane (Dieffenbachia seguine), Arum maculatum, Colocasia esculenta and Wisteria floribunda var. alba. Lectins with inhibitory activity against Herpes simplex (HSV) have been isolated from a number of natural sources. They include concanavalin A (from Canavalia ensiformis), and agglutinins from Soybeans, Wisteria floribunda and Narcissus pseudonarcissus. These compounds, which are active at a level that is below their cytotoxic threshold, are good candidates for anti-HSV research.
Xanthosoma sagittifolium. A lectin from Typhonium divaricatum has been of particular interest as a mannose-binding agent with anticancer and antiHIV activity that is well below the cytotoxicity (cell-damaging) threshhold (Luo 2007; Mo 1999; Van Damme 1995). Lectins from Alocasia indica have shown immune stimulating activities (Kamboj 1995), and a lectin with anticancer activity against cervical cancer cells has been isolated from A. cucullata (Kaur 2005). A lectin from Dioscorea nipponica has also shown pesticidal attributes (Ohizumi 2009).
The Amorphophallus Yams
The Elephant-foot Yam, Amorphophallus paeoniifolius (formerly A. variabilis or A. campanulatus), ranges from Australia to Indonesia and Malaysia, to Borneo and the Philippines. It is an attractive herb with a seasonal habit that dies down in the dry season. The spathe-like flowers emerge with the first rains of the wet season, with the umbrella-like leaf that is characteristic of the genus appearing later. Aboriginal people use the tuber, which can attain a respectable size, as a vegetable – wrapped in paperbark and cooked overnight in a ground oven (Yunupinu 1995). In some places more extensive preparation is undertaken: the thinly sliced tuber being washed in water for 24 hours before being roasted. Inadequately prepared, the tuber (or juice) is inedible – an unpleasant experience described as being ‘similar to eating glass shards’ (Wightman & Andrews 1989). Joseph Maiden mentioned that Amorphophallus variabilis leaves were smoked by the Aboriginals of the
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Northern Territory as a substitute for tobacco (Webb 1969). In Queensland the Yellow Lily Yam, Amorphophallus galbra (fruit, stem and root) has been utilised as a seasonal food resource (Roth 1901). In some areas of the Northern Territory this species, known as one of the ‘cheeky yams’2, was eaten in preference to the yam Dioscorea bulbifera and was said to have a more pleasant flavour. However, there are two tuber ‘types’ (or two stages of ripening), the use of which depended on a test of the vine: no exudation from the stem: the tubers were • replanted as they were considered to still have ‘cheeky’ properties; • watery juice exuding from the broken stem: the root was deemed edible. Certainly records of early experiences concur with its irritant reputation. In 1948 a scientific expedition to Arnhem Land mentioned cooking the tuber in a ground oven: ‘Until it has been sufficiently cooked this corm has a very sharp flavour and leaves an unpleasant burning feeling in the mouth’ (Isaacs 1994). The success of the cooking process, which took 3 to 4 hours in an earth oven, was gauged by tasting water samples from the yam to see if it still had ‘cheeky’ properties. The cooking continued until it was considered to have lost its irritant activity (Lindsay 2001; Marrfurra 1995). Henry Burkill (1935) mentioned the use of Amorphophallus root in China as a source of starch for making a bean curd substitute, while in Japan a form
2 The irritant attributes of the tubers were, like many of the Aroid family, due to their content of calcium oxalate crystals (which are found in all parts of the plant) – an irritant characteristic that earned them the name ‘cheeky’. However, some species contain additional toxic components.
177 Amorphophallus campanulatus, syn. A. galbra. Amorphophallus galbra (the species name has also been spelt glabra in some publications) is native to coastal regions of the Australian tropics: Cape York (northern tip) and the Northern Territory (Darwin area and offshore islands) ranging to Western Australia. (Image below courtesy: KAW Williams, Native Plants of Queensland, Vol. 4)
of vermicelli has been prepared from it. Burkill provided the following details of the use of Amorphophallus campanulatus in Malaysia and Indonesia, with an interesting explanation of the variability of the toxicity of these plants: ‘the tubers of the wild plant are very irritant, when raw, on account of the needle-like crystals of oxalate of lime, which abound in the tissues. It is reported that an alkaloid, allied to conicine [syn. coniine, a neurotoxic alkaloid], is also present in the tubers. In the cultivated races these needle-crystals are less abundant … Washing with prolonged boiling frees, in large measure, the wild tubers from the poisons, so they can be eaten. The cultivated roots are grown for no other purpose than eating.’ Burkill further noted: ‘No special preparation for eating is given, in Java, to the cultivated tubers. The Sakai eat the wild tubers in Malaya. Long washing
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after pounding and then prolonged cooking are necessary…. the tubers [are] crushed, dried and then cooked by the Semang of Upper Perak’. Amorphophallus variabilis was processed similarly in Java (Burkill 1935). In the Philippines the tubers of Amorphophallus campanulatus were not relished and were used only ‘in times of dearth’ – although they were fed to pigs after being sliced, sundried, pounded to a meal, and then boiled. The older petioles have also been used as pig food. In the Philippines the young petiole (before the blade expanded), peeled and parboiled, was considered to be a delicacy (Quisumbing 1951; Burkill 1935). Interestingly, in Papua New Guinea the inner part of the petioles was crushed to extract a juice that was fermented in bamboo rods, after which it was taken as a remedy for diarrhoea (Perry & Metzger 1981). A juice extracted from Amorphophallus campanulatus, which was said to have toxic properties, was used as an admixture with Antiaris toxicaria in potent dart-poison by the Semang of Perak, ‘1/10th part making the poison strong enough to kill a rhinoceros or tiger’ (Burkill 1935). Antiaris toxicaria on its own is highly toxic and the effect of the Amorphophallus juice was not clearly explained: ‘Wray looked on it as an addition for the purpose of preventing an animal getting away’, which implies a sedative effect. The juice from Amorphophallus prainii, again mixed with Antiaris latex, was also used as a dart-poison by the Semang (Burkill 1935). The fact that most preparation processes would inactivate the oxalate crystals suggests that other components were present in the preparation that attracted the interest of the poison-makers. Amorphophallus tubers have been utilised medicinally in India, China and Southeast Asia in a manner similar to those of the genus Typhonium. In particular Amorphophallus riveri (syn. A. konjac), which had a very poisonous reputation, was said to have anticancer properties. It has long been incorporated into formulas for treating encephaloma, thyroid and parotid gland cancers, lymphatic tumours and nasopharyngeal cancer (Chang 1992). The corm (made into a paste) was applied to rodent ulcers or poisonous snake bites.3 The plant has been used as an insecticide. The pungent black inflorescence (before flowering) was also used medicinally – as a febrifuge, for aching ‘creaking’ bones, and eye inflammation (conjunctivitis) (Duke & Ayensu 1985; Perry &
Metzger 1981). There appears to be some validity to these claims. Refined Amorphophallus konjac demonstrated experimental anticancer activity against lung cancer in mice – not only was there a significant drop in cancer rate and the incidence of precancerous lesions, there was an overall decrease in malignancies and survival times were prolonged (Luo 1992, 1991). The Elephant-foot Yam, Amorphophallus campanulatus (syn. A. paeoniifolius)4 has long been cultivated in Southeast Asia as a tuber crop. It had a medicinal reputation similar to Konjac as an antiinflammatory and antirheumatic agent in Indian medicine. The acrid tuber was a popular remedy for acute rheumatism and, in the Philippines, the caustic corms were applied locally as a rubefacient poultice. In India the prepared tuber (cooked and washed) was valued as a stomachic and carminative that was utilised for all manner of digestive disorders (dyspepsia, colic, flatulence) – as well as for treating dysentery, spleen and liver problems. In addition, it was regarded as being a useful remedy for respiratory disorders (coughing, bronchitis, asthma), menstrual distress (utilised as an emmenagogue; amenorrhoea, dysmenorrhoea), male seminal weakness, and as a tonic for fatigue, anorexia, anaemia and general debility. The roots were applied locally for boils and ophthalmia (eye inflammation) (Das 2009; Kapoor 1990; Chopra 1956). Indian traditions also mention that the corm pieces were fried in ghee and eaten for the treatment of piles (Silja 2008). In Indonesia the tuber poultice was placed on the abdomen for constipation (Hirschhorn 1983). The tubers could also be cooked with Allium (garlic) and Averrhoa bilimbi (Bilimbi/Cucumber tree) and smeared on calluses on the soles of feet (Perry & Metzger 1981). While this great diversity of recommendations may appear almost fanciful, a number of investigations have determined that Amorphophallus campanulatus tuber extracts had anti-protease, analgesic and cytotoxic properties – as well as interesting antioxidant and hepatoprotective activity. The polyphenolic components of the extract (including gallic acid, 3 Amorphophallus gigantiflorus has been applied locally to treat buboes, swellings, and ‘mad dog’ bites in Taiwan. It was also taken internally for diseases of the respiratory tract in Taiwan (Perry & Metzger 1981). 4 The name A. campanulatus is used in this text as it is the identification utilised by all the cited references – although today it is generally agreed that A. paeoniifolius is the correct term.
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resveratrol, quercetin) were of particular interest (Angayarkanni 2010; Jain 2009; Shilpi 2005). Recently, substantial effects on the central nervous system were demonstrated that involved muscle relaxant and CNS depressant activity (reduced locomotor activity and sedative effects). The activation of splenocyte (spleen cell) activity by a tuber polysaccharide has attracted interest for potential effects on immune system function (Das 2009a, 2009b). In addition, tuber extracts have shown significant antibacterial activity against a broad range of microorganisms, although the antifungal properties of the extract were fairly weak. The triterpene amblyone was found to be a highly active antibacterial component (Khan 2008, 2007). Amorphophallus campanulatus leaf extracts have shown activity against Aspergillus flavus – a potential hepatotoxic aflatoxin food contaminant. Calcium oxalate has also shown antifungal activity, while corm extracts were substantially less active (Prasad 1994).
A Titan Arum
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The flowers of Amorphophallus are of particular interest to the botanical world due to the aroma of rotting meat they utilise as a pollination strategy – which has led to the descriptive common names of ‘Corpse Flower’ and ‘Corpse Plant’. This attracts insects that are usually thought to be beetles, although they are more likely to be carrion flies. The Indonesian rainforest Titan Arum, Amorphophallus titanum, produces one of the largest flowers in the plant kingdom. It is impressive in blossom, with a massive inflorescence. The specimen here, which was photographed in January 2011 at the Cairns Botanic Gardens, is one of the few in Australia and has taken ten years Pollen inside the to produce a flower. The Titan Arum. (Image tuber can weigh a rather courtesy: TGray remarkable 50 kilograms. Photography, CCA by SA 3.0)
This image from the early 1900s (c. 1900–40) shows two Titan Arums in Sumatra, Indonesia, that illustrate the massive size of the leaf, which can reach up to 6 meters, as well as the flower. (Image courtesy: Tr o p e n m u s e u m of the Royal Tropical Institute, Amsterdam,
Konjac: A Large Tuber with a Big Commercial Future Amorphophallus titanum in bloom. This flower was 1.6 metres in height, and when fully open achieved a diameter of about 1.2 metres. (Courtesy: Rose Williams)
The large starchy root (corm) of Amorphophallus konjac is the source of the fibre-rich flour known as Konjac. The dried corm contains 49–60 per cent (w/w) glucomannan gum, a polysaccharide component that
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gives konjac jelly viscous attributes. The corms also contain starch (10–30%) and crude protein (5–14%). Lower levels of soluble sugars, vitamins and minerals are present, as well as small amounts of alkaloids (including trigonelline) and saponin. Serotonin (and derivatives) has been found in the fresh corms.5 However, like Taro and numerous other aroids, fresh Konjac root requires processing to remove the calcium oxalate component and other impurities (starch, protein, sugars) before it can be utilised as a food. Processed Konjac is a popular gelatin-like component in Asian cuisine, used in the making of noodles, tofu, and innumerable types of snacks. The Japanese shirataki and oden noodles, and the dishes sukiyaki and gyudon, are konjac- (konnyaku-) based (Chua 2010). 5 Serotonin (5-hydroxytryptamine is largely found in the gut (90%) and the remainder in the central nervous system. It is an important neurotransmitter that influences mood, appetite and sleep.
Konjac plant (Amorphophallus konjac). (Courtesy: Pekinensis, Wikimedia Commons)
Konjac Puff Sponge. (Courtesy: The Konjac Sponge Company)
Konjac Resources
Amorphophallus bulbifer.
The Voodoo Lily (Amorphophallus bulbifer) is native to India, the Himalayas and Burma. The tuber has been proposed as an alternative source of Konjac glucomannan. This is of interest because there are 163 species of Amorphophallus and, with only twelve species having been investigated for suitability as a glucomannan resource, it has good prospects for cultivation as a crop (Wang 2011). Liu (2004) lists the following, in addition to Amorphophallus konjac, as suitable resources for dietary and medicinal use: A. albus, A. corrugatus, A. kachinensis, A. krausi, A. nanus, A. paeoniifolius, A. yuloensis and A. yunnanensis. Some species are even considered suitable for wine production. However, not all Amorphophallus species are acceptable. An investigation of seven Amorphophallus species determined there were good levels of glucomannan (around 30%) in Amorphophallus albus, A. konjac, A. yuloensis, A. xemengensis and A. dunnii – while A. sinensis and A. yunnanensis were unsuitable (Li 1996). In Assam the Voodoo Lily (Amorphophallus bulbifer) has been listed as a medicinal weed in the crop fields, where the fresh rhizome provides a local remedy for treating piles (Bhattacharjya & Borah 2006). The petiole and bulbils have been utilised as a cooked
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vegetable, eaten with dry fish and rice, for 10– 12 days as a treatment for rheumatic, muscular or joint pain in northeast India (Tripura state) (Das 2009). The root of the herb has also been utilised for treating skin diseases by the Jaintia tribe in India (Kayang 2007).
A purified form of Konjac (konjac glucomannan) has gained favour as a dietary supplement and drink mix with a beneficial effect on obesity, bowel function and carbohydrate metabolism. Glucomannan, which is made up of mannose and galactose, is a polysaccharide-based soluble fibre that provides a useful intestinal bulking agent. Its recommendation as a treatment for obesity is linked to improved sensations of fullness and satiety, as well as physical benefits for bowel function.6 It directly increases faecal volume (which aids in the relief of constipation), slows intestinal transit time, promotes the removal of wastes (faecal matter) and reduces sugar absorption. Konjac glucomannan provides a prebiotic addition to the diet, which acts to boost lactic bacteria in the colon and improve fermentative food processing.7 The modification of sugar metabolism, and changes in the transport of cholesterol and bile acids, results in a significant hypocholesterolemic (reducing cholesterol absorption) effect. However, it is recommended that konjac glucomannan be taken separately from drug, herbal or nutritional therapies as it may modify their intestinal bioavailability – which could have beneficial, or detrimental, potential (Chiu 2010; Li 2005; González Canga 2004; Mao 2002)
6 With regard to the activity of soluble fibre, grain size can make a difference. Konjac flour that has been milled for a longer time has a smaller particle size and has shown a better anti-obesity effect (Li 2005). Experimental anti-obesity activity, which has been linked to reduced fat absorption and/or hypocholesterolaemic benefits, has also been demonstrated by the yams Dioscorea nipponica and D. tokoro (Song 2004; Kwon 2003). 7 Other dietary agents with similar prebiotic benefits include inulin and oligofructose, via their effect on lactobacilli and bifidobacteria, respectively (Yeh 2007). These dietary components are discussed in greater detail in Chapter 2.
181 Fenugreek (Trigonella f o e n u m - g ra e c u m ) . Soluble fibres have good cholesterol-reducing properties, although their efficacy can vary according to the chemical components. In addition to Konjac glucomannan, effective fibres include mannose-rich glucomannan from Dioscorea esculenta, and galactomannan from Fenugreek However, mannose-free arabinogalactan from Colocasia esculenta tubers only had a minimal effect (Boban 2006).
Konjac has a potential role in diabetic management due to its hypoglycaemic and hypoinsulinaemic effects – which probably involve a delay in gastric emptying and a slowing of glucose delivery to the intestinal mucosa. This, in turn, prevents raised blood sugar levels. Konjac has been utilised as a viscous gum additive in numerous food and drink products. It has stabilising and emulsifying effects suitable for use as a binding agent in meat and poultry products. However, there can be a few disadvantages for digestive function, resulting in flatulence and abdominal pain. Because the viscous gum can retain large amounts of water, there have been occasions where the swelling effect has caused oesophageal or lower gastrointestinal obstruction. Konjac has a firm consistency and does not dissolve like gelatine, making it more suitable for chewable snacks. There have been a few instances where a jelly has become lodged in the throat, resulting in airway obstruction – incidents that led to improvements in product design that now make this an unlikely scenario (Chiu 2010; Vanderbeek 2007; Li 2005; González Canga 2004; Chen 2003; Lu 2002). Even so, Australia has banned the importation of mini jelly cups containing konjac – a regulation that some companies do not appear to have been aware of, or have ignored (see www.productsafety.gov.au for details).
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Hypoglycaemic Effects of Dietary Starch The glycaemic index (GI) of foods provides an indication of their influence on blood sugar. Low GI foods are deemed more beneficial in the diet as they prevent rapid increases in blood sugar levels. Starch digestibility can significantly influence a GI rating – with easy digestibility tending toward higher GI due to a more rapid absorption. However, this can vary to a great degree. A comparison of different types of Yam is illustrative. The Chinese Yam (Dioscorea esculenta) rated higher digestibility (with the highest GI) in comparison to the lower digestibility (and lower GI) of three other species: Round-leaf Yellow Yam (D. cayenensis), White Yam (D. alata), and Lucea Yam (D. rotundifolia) (Riley 2008).
Puna yam, Dioscorea esculenta. (Courtesy: S Buchan, flickr)
Konjac has shown strong antibacterial effects against some microbial food contaminants, notably Escherichia coli (including enterohaemorrhagic E. coli), Salmonella enteritidis, Vibrio parahemolyticus and Staphylococcus aureus. It can also reduce levels of spore-forming bacteria (Bacillus subtilis and B. cereus, Clostridium perfringens and C. botulinum) (Kitamoto 2003). This is not only of interest to the food processing industry. The prebiotic effect of konjac glucomannan can increase beneficial bacteria (bifidobacteria, lactobacillus) levels in the intestine, with an associated antibacterial action in the colon reducing the bacterial load (Chiu 2010). Certainly, improved bowel function appears to be linked to a reduction in the incidence of colon cancer. Incorporating glucomannan konjac into the diet may well provide additional benefits (Yeh
2007). Studies have suggested that atopic disorders (eczema, dermatitis, asthma, allergic rhinitis) may benefit from an anti-inflammatory action, as well as an immune supportive effect (Chiu 2010; Onishi 2008, 2005; Kimata 2006; Oomizu 2006). For over 2000 years processed Konjac has been used medicinally for the treatment of respiratory disorders (asthma, cough), hernia, breast pain, burns, skin and blood disorders. It seems the ancient practitioners were right after all. There are various other suggestions regarding the use of Konjac glucomannan that are of interest. They include its use in pharmaceutical and personal care products, as well as cosmetics. It is one of the most viscous fibres known, due to its high water-retention capacity, and can be used in all manner of absorbable products, including disposable nappies and sanitary napkins. The market has extraordinary potential (Chiu 2010). The fibre has also been researched as a binding agent for slow-release drugs in the colon (Zhang 2006). In addition, the gum is an efficient plasma-expanding agent that may even have clinical usefulness as a plasma substitute. Other manufacturing applications mention its use for hazardous waste removal; in particular, it can act as a water-insoluble adsorbent to remove tannin from aqueous solutions (Li 2010; Liu 2010).
Aroid Toxicology
In Australia, both Cunjevoi and Taro have been implicated in incidents of Aroid poisoning. Eaten untreated they incite an immediate burning sensation in the mouth, the pain of which has been described as unbearable. This is followed by mucus membrane swelling. The intense pain continues until it eventually reaches a numbing type of insensitivity that is almost anaesthetic in nature. Gastrointestinal discomfort follows. Extremely painful eye irritation from contact with the sap has also been recorded. Some highly descriptive early accounts relate poisoning incidents. In 1929 Dr John MacPherson reported: At the inquest recently held on the death of a child after eating some ‘root’ of an arum or cunjevoi lily expert witness attributed death to the irritation of the mouth and throat by the needle-like crystals of calcium oxalate with which the plant abounded. This explanation seems to me utterly erroneous. Calcium oxalate, although sometimes its passage in the urine may give rise to pain and
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The European Cuckoo Pint (Arum maculatum)
Flower, leaves and fruit of the Cuckoo Pint (Arum maculatum).
The Cuckoo Pint (Arum maculatum) is a wild European herb with which James Cook, Joseph Banks and Daniel Solander would have been very familiar. Certainly they would have known of the toxic reputation of this plant – and of others with a similar appearance. The berries, which are produced in autumn, remain on display long after the leaves have withered away – an attractive looking juicy ‘berry’ that can entice children to experiment. Maude Grieve (1931) commented: ‘In spite of their very acrid taste they have sometimes been eaten by children, with most injurious results, being extremely poisonous. One drop of their juice will cause a burning sensation in the mouth and throat for hours. In the case of little children who have died from eating the berries, cramp and convulsions preceded death if no medical aid had been obtained.’
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haematuria [blood in the urine], is relatively innocuous and inert. In fact the treatment of oxalic acid poisoning is best effected by administering chalk, whiting, lime-water to some soluble calcium salt as a chemical antidote to precipitate the insoluble calcium oxalate.
Studies evaluating Taro (Colocasia esculenta) leaves have shown no significant differences in the amount of total oxalate or calcium oxalate between edible and non-edible cultivars (average 426 mg/100 g fw) – indicating that the acrid nature of the leaves was not only due to the oxalate content (Holloway 1989). Part of the explanation of the virulence of Aroid toxins involves the administration strategy utilised by the plant toxin. The needle-like calcium oxalate crystals (raphides) act as dart-like penetrating agents, piercing the skin to inject substances (such as enzymes) that cause tissue swelling, which primarily affect the mouth and throat. Symptoms of toxicity from ingestion of the plant leaf or tuber (raw or cooked) are generally a raw sore throat, with associated numbness of the oral cavity. Some individuals develop additional symptoms which can develop into extreme discomfort: salivation, swollen lips, dysphonia (difficulty speaking), ulcers of the oral cavity, difficulty in swallowing, abdominal pain and thoracodynia (chest pain) (Lin 1998; Chan 1995). The extensive preparation used by Aboriginal people would have been an essential prerequisite for the consumption of Taro and Cunjevoi. Despite the various opinions as to the desirability of the resultant dough, the end product was edible. Even so, another obstacle exists with regard to the use of these plants. Some varieties are cyanogenetic (containing varying amounts of cyanide), and extra care would be advised in their preparation.
The Oxalate Puzzle
There are soluble and insoluble forms of calcium oxalate crystals, a crucial consideration when evaluating a plant’s toxic potential. Insoluble crystal forms, such as those found in many Aroids, are not readily bioavailable in the body and systemic reactions are fairly rare, although some individuals are particularly sensitive. Treatment of calcium oxalate exposure (ingestion) involves a lot of fluids to ‘wash out’ the system and prevent the potential deposition of oxalate in the kidneys, muscles and bones. Sodium citrate (dose: 0.15 mg/kg per day) will also inhibit the crystallisation of calcium oxalate (Barceloux 2008).
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Oxalate Comparison for Yam Roots
Taro root and plant.
Fruit and vegetable juices containing citrate may be a helpful dietary inclusion for individuals prone to calcium stone formation. Tomato is a citrate-rich vegetable with a high content of magnesium and low levels of sodium and oxalate. Fresh tomato juice in particular would provide a concentrated form of citrate that could aid in the prevention of stone formation (Yilmaz 2010, 2008).
Cassava plant and root.
Taro leaves (Colocasia esculenta), Giant Swamp Taro stems (Cyrtosperma chamissonis), the Elephantfoot Yam (Amorphophallus campanulatus), and the skin of the tuber of the Giant Taro (Alocasia macrorrhizos), all contain about 10 times the amount of calcium oxalate (i.e. around 400 mg/100 g fresh weight) than is found in similar root crops – sweet potato (Ipomoea batatas: 32 mg), cassava (Manihot esculenta: 17 mg), Giant Taro tuber (Alocasia macrorrhizos: 31 mg), Taro (Colocasia esculenta: 43 mg), Xanthosoma: 23 mg) and yams (Dioscorea esculenta and D. alata:negligible levels). The difference in values for Giant Taro skin and tuber is due to the fact that the oxalate is concentrated in the outer layers of the corm and can be largely removed by peeling off a thick layer and prolonged boiling (Holloway 1989).
Oxalate is not a desirable food component as its presence can seriously compromise the nutritional value of some vegetables. Oxalate binds with a number of minerals, thereby limiting their bioavailability. However, the type of oxalate is an important consideration – it is the soluble form that is of concern for dietary purposes. The level can vary considerably in different vegetables, and with different cooking processes. The oxalic [sic] content of Taro can be fairly low (133 mg/100 g) in comparison to spinach (658 mg/100 g) and rhubarb (1336 mg/100 g) (Duke & Ayensu 1985). The calcium availability from highoxalate vegetables such as spinach is low (around 5%), while its availability in kale (a low-oxalate containing vegetable) rates much higher (41%). However, this is not always the case – soybeans (a high-oxalate food) can have good calcium bioavailability, possibly because soybeans contain phytate, which inhibits oxalate absorption (Al-Wahsh 2005; Franceschi & Nakata 2005; Heaney & Weaver 1990; Weaver 1987). Interestingly, studies have found that the calcium absorption from milk was superior to that provided by spinach (Heaney 1988). The solubility and absorption of calcium oxalate in the body can lead to kidney stone formation, and this makes the other factors that influence oxalate
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Dietary Oxalate
Beetroot plant (Beta vulgaris cultivar). The levels of phytate in Soybean (Glycine max) can vary substantially; high-phytate, low-oxalate cultivars are desirable. The oxalate content of soy-based foods is equally variable. Commercial soy foods can contain between 16– 638 mg of total oxalate per serving (Massey 2001). When soybeans are processed to make tofu, most of the oxalate appears to be bound to calcium and magnesium, which are insoluble, making the oxalate unavailable for absorption. Overall, therefore, the absorption of soybean oxalate tends to be very low (2–5%) (Massey 2007). (Image courtesy: Herbert Zell)
bioavailability from the diet important.8 They include pH, fibre consumption and mineral levels (notably calcium, magnesium and phosphate) – as well as a gut bacteria (Oxalabacter formigenes) that utilises oxalate and thereby determines the amount of free oxalate in the colon. A higher dietary intake results in elevated urinary excretion, thereby increasing the likelihood of crystal deposition in the urinary tract. The retention of dietary oxalate can vary substantially (24–53%: based on a variable intake from 10–250 mg/day), with even a small amount raising the risk of stone formation in susceptible individuals (Franceschi & Nakata 2005; Massey 2007, 2005).
8 In addition to oxalate, calcium can combine with other substances – calcium phosphate and/or calcium carbonate – to form stones. While calcium stones are the most common, there are other forms of kidney stones: cystine stones form in people suffering cystinuria (a hereditary disorder involving too much cystine in the urine). Stones that develop from struvite (ammonium magnesium phosphate, a mineral) occur in recurrent urinary tract infections, while uric acid stones are associated with gout or chemotherapy.
Swiss Chard (Beta vulgaris var. cicla). (Courtesy: Jonathunder, Wikipedia)
Investigations of common vegetables indicate soluble oxalate levels can range from 39–83 per cent. Beetroots, Brussels sprouts, carrots, potatoes, spinach, red and green Swiss chard leaves are the main vegetables with high soluble oxalate levels (above 60%). Broccoli and rhubarb stalks are low in oxalate. However, the cooking process employed can make a dramatic difference to the oxalate content of these vegetables (Chai & Liebman 2005): Boiling was extremely effective at reducing • oxalate content (30–87% reduction). However, even after boiling some vegetables could retain high oxalate levels – i.e. spinach, Swiss chard leaves, rhubarb – even though there had been fairly good losses during the process (61–87%). The oxalate loss in potatoes (skin removed)
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during boiling was 34 per cent. • Boiling can also reduce insoluble oxalate in some vegetables (rhubarb stalks, Swiss chard leaves, broccoli, Brussels sprouts: 15–74%), but not in others (spinach, beet roots). • Steaming was less effective (6–19% oxalate reduction), although the loss for carrots, green Swiss chard and spinach were fairly good (42– 53%). • Baking, which would only be useful for root crops (in this study potatoes were examined) was the least effective, having little effect on oxalate levels.
Oxalate Comparisons The soluble oxalate levels in Taro (236 mg oxalate per 100 g wet matter) is comparable to other green leafy vegetables (per100 g wm): spinach (Spinacia oleracea 266 mg), silverbeet/Swiss chard (Beta vulgaris var. cicla 252 mg). However, alterations in oxalate depend on preparation Taro leaves. methods (Savage & Dubois 2006; Brogren & Savage 2003): • Soaking Taro leaves for 30 minutes, or baking the leaf, made only a marginal difference to oxalate levels. Prolonged soaking (18 hours) reduced the content in uncooked leaves by 26 per cent. • Boiling the leaves was the most effective form of preparation as it reduced soluble oxalate by 36 per cent. Insoluble calcium oxalate levels in the leaves remained largely unchanged: raw leaves (178 mg) and soaking leaves for 18 hours (168 mg). The mean insoluble oxalate level of cooked (boiled, baked) Taro leaves was high (250 mg wm). Oxalate levels in silverbeet and spinach (mg/100 g wm) (Savage & Dubois 2005): Insoluble oxalate: raw silverbeet leaves (273 •
mg); raw spinach leaves (63 mg). • Boiled silverbeet (173 mg); boiled spinach (64 mg). Oxalate levels in frozen spinach (Brogren & Savage 2003): • High soluble oxalate levels: (736.6 mg +/-20.4 mg). • Levels of insoluble oxalate were comparable to Taro (220.1 +/-96.5 mg). • Frozen spinach calcium levels were quite good (90 mg total calcium/100 g wm). However 76.7 per cent was unavailable due to its binding as insoluble oxalate. The addition of a low-fat milk or sour cream was found to substantially reduce oxalate content in vegetables such as spinach and silver beet (Simpson 2009). Hence, consuming a high-calcium milk product can bind oxalate, making it unavailable for absorption (Savage & Dubois 2006). Magnesium is equally useful for binding oxalate. This consideration is particularly important for those who tend to produce oxalate-based urinary tract stones. Amaranth (Amaranthus gangeticus) is a potent inhibitor of calcium absorption due to its high oxalate content and should be avoided by individuals with urinary tract stones or osteoporosis (Larsen 2003). (Image courtesy: Toshiko, flickr)
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Turmeric (and Cinnamon) have become popular spice additions to the diet as they can lower cholesterol absorption and improve blood sugar control. However, some spices can contribute to absorbable oxalate levels, thereby increasing the risk of urinary Turmeric, fresh rhizome. tract stones. Turmeric was found to be a high oxalate containing spice with significant levels (92% absorbable oxalate) in comparison with Cinnamon (6%) (Tang 2007).
Raphide Crystals
Calcium oxalate raphides. chinesemedicinetimes.com)
(Courtesy:
www.
The calcium oxalate crystal content of a plant is involved in calcium regulation strategies. This can provide a measure of tolerance to the heavy metals (aluminium, lead, strontium, copper, cadmium) that limit or damage plant growth. The stinging hairs are well designed – they contain crystals with a single groove that can transport a toxin into a puncture wound. However, oxalate crystals come in a variety of forms, some of which are unique to a genus. Aroid crystals often take the shape of needle-like raphides (which occur in bundles) and/or druses (multiple crystal faces form around a central axis) – although other
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crystal forms include styloids, prisms and crystal sand. There can be generic differences in raphide design. Araceae raphide crystals may have a highly unusual grooved H or dumb-bell appearance when viewed in cross-section, such as those found in Amorphophallus and Xanthosoma sagittifolium. Raphides found in Colocasia, Alocasia and Pistia may have barbs near their tips and along their edge (reminding one of some fishing spear designs) (Prychid 2008). A similar style of raphide from Pinellia (P. ternatea, P. pedatisecta) showed a sharper edge, in comparison to those found in Arisaema amurense and Typhonium giganteum. However, calcium oxalate monohydrate is not the only toxic component found as Aroid raphides, with the toxicity level of some raphides around 200 times greater than that of the crude drug (Wu 2010). This suggests that processing methods such as those used in Chinese herbal medicine can be extremely effective at reducing toxicity. Many Aroids contain poisonous compounds that have not yet been fully identified. Toxic reactions appear to result from a combination effect that not only involves calcium oxalate crystals – there are other irritant chemicals in these plants. Dr John MacPherson mentioned this consideration in his 1929 report on the death of a 4-year-old child: ‘The arum lily and cunjevoi … all parts of these plants … contain an intensely acrid and irritant poisonous principle which is volatile and soluble in ether … This was the constituent, doubtless, which caused the child’s death.’ Numerous unidentified chemicals may be responsible for the variations in Aroid toxicology. For instance, substances named sapotoxins have been detected in Taro and a species of Xanthosoma (X. atrovirens). The sapotoxin in Alocasia macrorrhizos can cause gastroenteritis and nerve paralysis, and neurotoxic effects have been confirmed experimentally. The full pharmacology of these poisons remains unknown. Their volatile nature has been a significant obstacle to biochemical investigations. It is thought that the mucilaginous nature of the mixture may also act as a vehicle, whereby the toxins elicit a more intense reaction, or that the chemical reaction may
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actually make the mucilage itself poisonous (Lin 1998; Chan 1995).
Cocoyams: Poison or Provender?
the Elephant’s Ear (X. caracu), and Malanga or Tannia (X. sagittifolium). Their tubers have been utilised in the West Indies, tropical America and the Far East (Morton 1982). A comparison of the flour prepared from Malanga and Taro tubers showed they were very similar9, with the Cocoyam having a higher starch and sugar content, while Taro was higher in fat, fibre and some minerals (phosphorus, calcium, iron, zinc) (Perez 2007).
Cocoyam root. (Courtesy: Xanthosoma sagittifolium, www.cocoyam.com) Cocoyam leaf.
There are about 50 different species in the Xanthosoma genus, which is found from Mexico to tropical South America and the West Indies. These herbs all possess large attractive leaves, a feature which has made them a popular ornamental throughout the tropics. The Tall Elephant’s Ear or Yautia Palm
(Xanthosoma jacquinii) provides a good example of a species with a highly virulent toxic reputation that has ensured it is never used as food, not even in times of desperation. One case history mentioned sampling a teaspoonful of Xanthosoma jaquinii after the tuber was twice-boiled. Despite the fact that the woman involved did not swallow the sample due to its unpleasant (tough, stinging) character, even this small taste was enough to irritate the throat and oesophagus. Even after three weeks the tissue damage had not fully healed and her voice had not returned to normal (Morton 1982). Numerous other Xanthosoma species have been implicated in toxic reactions – although there are a few edible species known as Cocoyams: the Purple-Stemmed Elephant’s Ear (X. nigrum), the Blue Taro (X. violaceum),
Blue Taro (Xanthosoma violaceum).
There appears to be only a limited amount of information with regard to the medicinal potential of the genus. The use of a species as a snakebite treatment by the Ketchwas people in the Amazon suggests detoxicant or anti-inflammatory potential (Schultes & Raffauf 1990). Leaf extracts of the Cocoyams Xanthosoma violaceum and X. sagittifolium have demonstrated antioxidant properties which were linked to their carotenoid and phenolic components (Arruda 2005, 2004; Picerno 2003). In addition, these yams have antimicrobial potential. Extracts of Malanga have shown significant antifungal activity, while sterols (hydroperoxysterols) from 9 In some places Taro (Colocasia esculenta) has also been known as Cocoyam or Water Cocoyam.
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Xanthosoma robustum exhibited antibacterial activity against Escherichia coli, Bacillus subtilis and Micrococcus luteus (Kato 1996). Malanga extracts have antifungal activity against the yeast Trichophyton rubrum, the fungus responsible for athlete’s foot and ringworm (Schmourlo 2005). In addition, there is an interesting study indicating that Cocoyam (Xanthosoma sagittifolium) was superior to barley or sorghum for brewing beer due to its higher carbohydrate content. The beer, which was of a dark bitter type, was deemed to have good commercial prospects (Onwuka & Eneh 1996). The poisonous nature of a number of Aroids has over the centuries led to a few less than desirable practices – some of which involve serious malicious intent. Alocasia denuda, which had a particularly virulent reputation, was once employed in a dart poison on the Malay Peninsula. It was supposed to act as an irritating additive to the main poisonous mixture, although the processing involved may have reduced its toxic value. It was certainly thought to be a successful contact poison. Powdered and mixed with bamboo hairs, it caused severe itching if rubbed on the skin. If used to spike food it was said to result in a painful death (Perry 1980 & Metzger; Burkill 1935). The root of Alocasia montana had the more unusual reputation of being a tiger poison (Quisumbing 1951). It has been stated that Cunjevoi (Colocasia macrorrhiza) juice was used by Aboriginal people in Australia to poison their spears, but its effectiveness is doubtful (MacPherson 1929). Likewise, despite its reputation as a fish poison, tests established that it was not effective (Hamlyn-Harris & Smith 1916). Of all the Aroids, the Dumbcane (Dieffenbachia seguine and related species) has the reputation for the greatest toxicity. The chemistry of the genus, like most of the toxic aroids, is unclear. Certainly, the presence of calcium oxalate on its own does not account for the plant’s virulence. Other compounds that are present may include trypsin-like enzymes and proteases.10 The fresh juice of the stalk has the most irritant effect, although the toxins are fairly unstable when exposed to air or heat. Chewing the fresh plant results in
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maximum exposure to the chemical irritants as the needles of calcium oxalate are broken and penetrate the delicate mucous membranes of the mouth (Barceloux 2008). However, the level of calcium oxalate can differ according to the species: Dieffenbachia picta (whole plant 0.21%; juice 0.10%), and D. exotica (whole plant 0.37%; juice 0.15%) – suggesting species differences in toxic potential (Fochtman 1968). Clove oil is primarily composed of eugenol (72– 90%), which has significant anaesthetic and antiseptic properties. This would appear to give it good antidotal properties as there is experimental evidence that eugenol essential oil (from Caryophyllus aromaticus, syn. Syzygium aromaticum) can inhibit tongue oedema induced by Dieffenbachia picta. The effect was found to be substantially better than the standard emergency treatment, and not simply because eugenol acted as a natural NSAID – its analgesic properties also acted to block neurotransmission in the damaged tissue (Dip 2004, 2011). Conventional medical treatment normally involves local cleansing (rinsing out the mouth), the use of analgesics, possibly steroids and/ or antihistamines in moderate to severe cases. The use of Clove oil therefore provides a very good household remedial alternative.
Medicine bottle, Oil of Cloves, dispensed by O’Brien’s Pharmacy, Leichhardt, New South Wales, Australia (1940– 1960). (Courtesy: Powerhouse Museum, Sydney) 10 Proteases are a class of enzyme that catalyse protein breakdown (proteolysis) and are involved in numerous metabolic processes. Early studies isolated a proteolytic enzyme designated dumbain, as well as a cyanogenetic glycoside, from Dieffenbachia (Walter 1967). However, the effect of these compounds can vary substantially. Dieffenbachia maculata possesses significant proteolytic activity (particularly the stem) – with different parts of the plant demonstrating different types of protease enzyme activity (Chitre 1998). The fact that these compounds can have detrimental consequences is illustrated by a metalloproteinase from Dieffenbachia seguine that has been shown to cause fingertip necrosis (Mirastschijski 2010).
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The Notorious Dumbcane: Infamous Herb of the Slave Trade
Dieffenbachia seguine, Dumbcane.
Perhaps the most notorious of the Dieffenbachia genus is the popular potplant Dumbcane (Dieffenbachia seguine, syn. D. maculata) – a herb with a very shady past. The common name refers to its former use as a nasty form of torture to compel obedience in slaves. In 1707 the eminent physician and naturalist Sir Hans Sloane wrote: ‘If one Cut this cane with a Knife, and put the tip of the Tongue to it, it makes a very painful Sensation, and occasions such a very great irritation on the salivary Ducts, that they presently swell, so that the person cannot speak, and do nothing for some time but void Spittle in a great degree, or Salivate, which in some time goes off, in this doing in a greater degree, what European Arum does in a lesser, and from this its quality, and
being jointed this Arum is called Dumb-Cane.’ The toxin irritates the vocal cords and the person is unable to speak, often for several days – in severe cases death occurs from suffocation. It has other particularly unpleasant consequences due to corrosive burns of the digestive tract (mouth, throat and stomach). Sap entering the eye is equally hazardous, causing immediate and intense pain, watering and spasm of the eyelid. This results in massive swelling, persistent distressing pain, and abrasive injuries to the cornea of the eye. In severe cases of poisoning complications include respiratory failure, bradycardia (slow heart beat), hypertension, muscle twitching, cramps, and gastrointestinal distress (vomiting, diarrhoea). Unlike Cunjevoi (Alocasia macrorrhizos) the toxic substances in Dumbcane are not destroyed by heat. It is interesting that, in the Amazon, some Indian tribes utilised Dumbcane juice mixed in arrow poisons (with curare), although no comment is made as to how effective the mix would have been (Arditti & Rodriguez 1982). In the traditional medicine of the West Indies, Dumbcane had a few limited applications. The acrid juice-containing leaves were used as a counter-irritant for rheumatism. They could be employed raw, pounded into a poultice, or boiled with oil, for application to the aching or painful area. Sir Hans Sloane noted: ‘The Root is of more force than the Fruit or Leaves … Fomentations are made of them against Inflammations and Obstructions of Hypochindres [sic; hypochondres refers to liver and spleen] and Reins [kidneys]; and the Oil is good against those Evils … The Roots sliced and boiled in Wine, made into Baths, and used to the Feet, it is of great use against old and late gouts.’ The latter recommendation was thought very to be effective, as was the deployment of pieces of stalk infused in baths or in poultices for oedema (swelling) of the leg. Dieffenbachia was also used to treat dropsy (fluid retention causing swelling), sexual impotence and frigidity. There are other traditional medicinal uses
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of the plant that are quite diverse, primarily utilising it as an anti-inflammatory and antispastic agent (Arditti & Rodriguez 1982).
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significant changes in hormonal levels and temporarily inhibited ovulation (Costa de Pasquale 1984).
Homeopathic outline of the applications for Caladium seguinum (which is an old term relating to Dieffenbachia seguine, syn. D. maculata). From Dr SR Phatak, Materia Medica of Homoeopathic Medicine, 1977.
The herb has been used to induce temporary sterility in both men and women. In the past Dieffenbachia seguine was chewed in the Caribbean Islands to induce male sterility, an effect which was said to last 24–48 hours. It seems to be a rather tortuous method of contraception, but one can only assume there was some trick to the preparation that was not made public knowledge. Particularly horrifying was the use of Dumbcane in Nazi concentration camps in experiments to induce sterility, a frightening misuse of medical and chemical knowledge. Originally it was ‘discovered that the juice of .... Caladium seguinum [Dieffenbachia seguine] swallowed or injected, produces … after a certain time, particularly in male animals, but also in females, a lasting sterility’ (International Military Tribunal, Nuremberg 1946). Fortunately the experimenters were unable to cultivate the plant in large enough quantities to continue the testing and the trials were abandoned. In 1972 experiments showed fresh juice rendered male rats sterile for 40–90 days and female rats for 30–50 days. More recent research investigating the contraceptive effect of the plant showed that it produced
Dumbcane leaves in an ornamental planting.
Therapeutic ‘Elephant Ears’
There are diverse medicinal reports that mention the therapeutic use of Cunjevoi. Ron Hamlyn-Harris and Frank Smith noted in 1916: ‘It must be regarded as of great general utility by the aborigine, for Roth and others mention that the rootstock is eaten after preparation, and the modern blacks regard the roots, crushed and heated as a useful application in syphilis.’ Early settlers in Australia applied the leaf juice to relieve sunburn (taking great care not to get any in the eye), and the stems were useful for ulcerated sores. The leaf poultice was reputed to be effective for pain relief such as that associated with arthritis (Cribb & Cribb 1981). The chopped-up roots and leaves of Cunjevoi were used similarly for treating joint pain in Java. Indonesian and Indian medicine have also utilised a range of Alocasia-based treatments that generally employ the herb as an external stimulant for a rubefacient effect (Quisumbing 1951).
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A Weedy Ornamental
Calla or Arum Lily.
The Calla or Arum Lily (Zantedeschia aethiopica) is a lily-like Aroid from South Africa that has become a popular ornamental. Unfortunately, it can become a weedy escapee with invasive tendencies and a penchant for wetland areas. The plant has also successfully infiltrated rubbish dumps, which can be problematic as this can provide an easy opportunity to expand its range into native bushland. This has led to its classification as a noxious weed in Western Australia, where it has infiltrated pasture lands (Lamp & Collet 1996). As with most Aroids, the Calla Lily is considered toxic due to its calcium oxalate content. In addition, it can cause oropharyngeal (mouth and throat) irritation and acute gastroenteritis. If the resultant diarrhoea continues unchecked, death can result from exhaustion and shock. Fatal poisoning has occurred in children who have eaten the decorative white spathe or the yellow flower spike. However, because heating the leaves or rhizomes will reduce its irritant activity, it has occasionally been used in Africa as a starch resource and vegetable.
The name ‘Elephant Ears’ mainly refers to the Aroids Taro and Cunjevoi although, occasionally, it is used to describe some species of Xanthosoma (which are better known as Cocoyams) and Caladium – the latter referring to a range of ornamental houseplants also known as ‘Angel Wing’ or ‘Heart of Jesus’. All have the same potential for oxalate poisoning. Interestingly, the False Morel Fungi (genus Gynomitra) have also been known as ‘Elephant Ears’, although the names Beefsteak or Brain Mushroom are probably more common.
The plant appears to have had only a few medicinal uses, which are very similar to that of Taro. The fresh leaf, warmed, could be applied to sores, boils, insect bites and to painful body areas affected by gout and rheumatism. In Mexico the leaf juice provided a burn remedy. Extracts of the root, leaf and stem have shown antibiotic activity, which helps to explain some of these uses. An alkaloid called etiopine has been isolated from the leaf, stem and flower extracts. The related species Zantedeschia hastata was once used by Zulu women to avert repeated miscarriages, and was reputed to prevent small, weak babies (Plowman 1969; Watt & BreyerBrandwijk 1962). Throughout Asia and the South Pacific Taro and Cunjevoi have been widely utilised to promote wound healing. In Malaysia, wounds were bound with a mix of the leaves and moist sugar. The crushed or sliced tuber could easily be prepared as a poultice (used alone or with other ingredients) for application to swellings, sores or boils. It also provided an antiparasitic skin remedy useful for scabies, or a wash for ‘diseased palms of hands or soles of feet’ (Perry & Metzger 1980). In The Toxicology of the Arum Lily and Cunjevoi Lily, Dr John MacPherson provided an extensive
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summary of the use of Cunjevoi in skin disorders and wounds in Australia. These remedies closely reflect the deployment of the plant in many other countries: ‘A leaf, warmed over a fire, is said to relieve the pain and expedite the healing of burns and scalds. The leaves also enjoy popular repute as curative if kept applied to cuts or furuncles. Sores and ulcers, even of long standing, whether following injury or not, are said to be cured by prolonged application of the leaves. Cunjevoi is said to be the best remedy for “north coast itch” in horses.11 For this purpose the plant should be well boiled and the horse thoroughly washed with the extract twice daily. The disease will be cured within 6 weeks, but may return the following season.’
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black rot fungus12 (Masui 1989). Further studies may well discover other antimicrobial substances that could explain many of the folk uses of the plant. In Taiwan and China, Alocasia cucullata leaves were similarly used for wounds and ulcers, and the plant as an antirheumatic remedy (Perry & Metzger 1980; Burkill 1935). Alocasia odorata has a similar reputation in Chinese medicine, the pounded tuber being poulticed on swellings. The stem was also recommended as a remedy for gastrointestinal dysfunction (colic, stomach ache, cholera) (Duke & Ayensu 1985).
Alocasia odora is an Asian species commonly called the Night-scented Lily or Giant Upright Elephant Ear. The stem has been utilised in Vietnamese cuisine as a vegetable: peeled and boiled, then frozen, bagged or canned for use. (Image courtesy: Hector Garcia, flickr) The Australian Goanna (also known as the Monitor or Lace Lizard, Varanus varius) was believed to eat Cunjevoi leaf as a cure ‘after being bitten in an encounter with a venomous snake’ (MacPherson 1939).
Taro has likewise been a popular remedy for boils and ulcerous sores. On the New South Wales north coast (Tabulam and Lismore) the young leaves were fire-heated and the leaf veins lightly crushed. The hot leaf was then applied to the affected area (Webb 1969a). The soothing mucilaginous nature of the herb may partly explain this use, as well as a slightly astringent effect. Preliminary studies have found antifungal compounds in a species of Taro (Colocasia antiquorum) that were active against 11 Also known as Queensland itch; a seasonal allergic reaction to bites from small flies or midges that causes scabs and intense irritation, to the extent that a horse can completely rub off its mane and tail. Another old remedy was lard and sulphur mixed. Urtica cream and Calendula oil would probably work as well. 12 Alocasia macrorrhizos rhizomes contain an antifungal protein (alocasin) active against Botrytis cinerea, a fungus that is best known for infecting wine grapes and aiding in the production of a sweet dessert wine (Wang & Ng 2003).
These plants have been officially recognised by traditional Chinese medicine for centuries. Their use as folk remedies has been known since before the Han period – the second Imperial Dynasty of China (206BC – 220AD). Several species of Colocasia (T’uchih), as well as Cunjevoi, Alocasia macrorrhizos (HaiYu), have been cultivated in China. The seeds were used to treat indigestion, flatulence and disorders of pregnant women. A wash (seed decoction) was regarded as useful for pediculosis (lice). The leaves and stalk were used similarly – and as an external treatment for insect bites or other types of poisonous stings. Cunjevoi has an anti-toxic reputation for ‘disintegrating masses’, which permitted its effective use as an external treatment of boils and carbuncles. Additionally, it has been used to disperse stagnation and resolve scrofula (tuberculosis of the lymphatic glands in the neck). This has led to its use by AIDS patients for lymphadenectasis – a condition where the lymph glands are enlarged due to an increased amount of lymphatic fluid circulation (Zhong 1992).
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Scrofula: A Mycobacterial Infection
royalty was not bestowed lightly! The German physician Robert Koch discovered the causative agent in 1882, which was spread by saliva. The bacterium was also spread by inoculation (e.g. a knife or syringe wound if the blade was contaminated with spittle) and from eating infected products (e.g. milk). Drug-resistant forms of tuberculosis have become an ever increasing medical problem, particularly in the crowded city confines. The incidence of tuberculosis is rising, with an estimated 10.2 million new cases per annum reported in 2004–05, a substantial increase over the 8.4 million new cases recorded in 1999.
Henry IV of France ‘curing’ scrofula. Illustration by Andre du Laurens, 1609.
The use of Cunjevoi and Typhonium giganteum in Chinese medicine as a detoxicant for scrofula is interesting as it suggests these herbs have antibacterial attributes. Scrofula (an enlargement of the neck glands) was usually associated with the wasting disease once known as ‘consumption’ – which refers to tuberculosis (a group of disorders due to Mycobacterium tuberculosis). This condition was renowned for is effects on the lung, as it was commonly associated with a painful wracking cough, and ‘wasting syndrome’. It was familiar to the ancients, and Hippocrates (460–365 BC) called the condition ‘phthisis’. However, other body systems were affected as the mycobacterium spread via the lymphatic system – the intestines, skin (lupus vulgaris, a disfiguring skin disease), joints, bones, spine and meninges (meningitis). It usually manifested as scrofula (although other glandular tissues could be affected), and the term ‘king’s evil’ was once used to describe the disease. This was not (as one might expect) because it could mimic a disease associated with royalty, but referred to the belief that the king’s touch could cure persons afflicted with with the disease. However, one would imagine that once the supplicants had coughed all over the royal personage (thereby spreading the germ) they would suffer similarly. No doubt, the touch of
Aroids have shown antimycobacterial potential. Colocasia odora (syn. Alocasia odora) has been utilised as an anti-tuberculosis agent and treatment for pneumonia in China (Southwest School of Botanical Medicine 1975). Extracts of the African species Amorphophallus bequaertii have shown growth inhibitory activity against Mycobacterium tuberculosis (Tshibangu 2002). In addition, Alocasia longiloba has been applied to suppurating sores in cattle and recommended for ‘abdominal ills’ – remedies that suggest this herb has antibacterial properties (Perry & Metzger 1980; Burkill 1935).
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Cunjevoi’s anti-toxic reputation, as well as its anti-oedema and anti-inflammatory properties, supports the use of the plant (leaf, stem or tubers) for treating rheumatism, snake and insect bites (Lou 1987; Hong Kong CMRI 1984). This is interesting with regard to its use by Aboriginal people in Australia – the leaves or stems were pounded and applied to the bites and stings of snakes, stingrays and insects. There have been investigations of Alocasia that suggest similar efficacy for the treatment of venomous bites. In particular, studies of Alocasia cucullata, which is a snakebite remedy, have shown that extracts inactivated snake venom (Mors 1991). Further investigations demonstrated antidotal and protective actions against snake venom in mice. It was effective against Cobra and King Cobra venom, and had some protective action against that of the Silver-banded Krait. However, it was not useful for venoms of the Pit Viper or Moccasin species (Martz 1992). In Africa Colocasia antiquorum is similarly utilised for treating snakebite and rheumatic disorders. Studies have supported anti-inflammatory and anticholinesterase properties for tuber extracts – which contained good levels of gallotannins, but not condensed tannins (Fawole 2010). The toxicity of Cunjevoi in Chinese medicine has been well recognised. Even harvesting the rhizome must be undertaken with care and gloves are worn to prevent skin irritation. Medical texts record side-effects from the use of the inefficiently treated herb: numbness of the tongue and potential central nervous system intoxication. The antidote recommended in mild cases was rice vinegar or raw ginger. Preparation of the tuber is very similar to the detoxification procedures used throughout Southeast Asia and Australia. The tuber is peeled, sliced and soaked in water for 5–7 days (with frequent changes of the water), then sun dried. The fresh herb (greens) is prepared somewhat differently. It is fried with rice (until the rice burns), water added, the mix heated until the rice softens and the residue removed before use. In addition, the herb has been valued as a febrifugal agent and was employed to reduce high fevers such as those of influenza or typhoid. (It has been similarly used in treating fevers in India.) Conjevoi has also been recommended as a treatment for tuberculosis (Hong Kong CMRI 1984).
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Anticancer Aroids Taro and Cunjevoi leaves have been traditionally utilised in the treatment of cancer. In traditional Chinese medicine Colocasia esculenta has a reputation for ‘softening the hard’ which has led to its use in many forms of ‘growths’ and masses. Dai Zhao Zhang, in The Treatment of Cancer Alocasia macrorrhizos (syn. by Integrated ChineseA. indicum). (Courtesy: Western Medicine (1989), Fanghong GFDL) comments: ‘This is also effective [in the treatment of cancer]. It belongs to the same family of plants as Rhizoma Pinelliae and Rhizoma Arisaematis which are commonly used in the treatment of tumours by Chinese Herbs. Colocasia esculenta can also be used with other herbal ingredients in the manufacture of pills.’ The antioxidant properties of these herbs may have an influence their cellular protective, anticancer and anti-inflammatory potential. Indian studies have evaluated the antioxidant attributes of Alocasia macrorrhizos (rhizome, roots, leaves) and A. fornicata (leaves, stolons) (Mandal 2010). Leaf extracts of Alocasia indica (a synonym for A. macrorrhizos) have shown significant hepatoprotective effects and antioxidant activity (Mulla 2009a, 2009b).
Alocasia crassifolia (syn. A. alba) is a large-leafed Asian species that has been utilised similar to Taro and Cunjevoi as an antitumour, analgesic, anti-inflammatory, antioedema and detoxicant remedy.
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to yield a starchy paste. This can be left to naturally ferment and produce ‘sour poi’. The predominant bacterium in poi is Lactococcus lactis (95%), with a small amount of Lactobacilli. Poi has been a popular foodstuff throughout Oceania, Papua New Guinea and parts of Asia, particularly Indonesia and Malaysia.13 In Hawaii it was formerly a staple dietary item in hospitals that was regarded as being very useful for allergic individuals (particularly children), infants who failed to thrive, and those suffering from gastrointestinal disorders such as inflammatory bowel disease, gastroenteritis and food intolerances. Certainly those intolerant of grains (such as wheat, corn and rice), soybeans or milk products could use poi as a low-allergic alternative. In addition, for individuals suffering coeliac disease poi has potential as a gluten-free alternative to wheat products. Poi has a low protein content, is easily digestible (the starch granules are very small), and its mineral component is readily absorbable. It has an alkaline influence on the A Probiotic from Poi? digestive system due to its potassium, sodium, calcium and magnesium content. Suggestions have been made that these dietary benefits may be of use for a diversity of conditions associated with dig-estive malfunction: pancreatitis, cancer cachexia, AIDS, poor immune function and lactase digestion problems (Brown & Valiere 2004). Studies have yet to be undertaken to fully Hawaiian men pounding poi, c. 1890. From Historic Photographs of Old Hawai’i (1820s evaluate the potential to 1940s). benefits of this traditional corm starch. Poi is prepared from the cooked and mashed 13 In Papua New Guinea another traditional fermented Taro dish known as Sapal has been prepared utilising Taro corm and coconut corms of Taro (Colocasia esculenta), to cream. Fermentation occurs naturally due to lactic acid bacteria (primarily which water is added and the mix strained Leuconostoc mesenteroides or L. aramesenteroides) (Gubag 1996).
Taro’s medicinal use in India reflects a similar antibacterial and healing reputation. The juice extracted from the stalks provided an astringent remedy that was effective for the treatment of ear infections (otorrhoea) in children. Simply putting the fresh leaf on sores was claimed to heal even difficult cases associated with chronic infection. Its styptic activity was famous, leading to its popular use as an anti-haemorrhagic agent. One of the more unusual claims involves a particularly unappealing treatment for toothache in the Philippines – where a small package containing a mix of decayed leaf-stalks and hot coals was applied to the troublesome site (Quisumbing 1951). The stems of Alocasia indica were applied to skin infections in India and Java, while the boiled stems could be taken as a mild laxative (Burkill 1935). This species was used in Fiji as a remedy for stomach ache and diarrhoea. In Papua New Guinea a headache remedy involved rubbing the sap and young leaves into the head. More unusual is the treatment for sexual insufficiency, where the leaves were cooked in coconut milk and eaten (Weiner 1985).
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Recent studies have provided some indication as to the potential dietary benefits of Taro. Studies of the anti-cholesterol potential of Colocasia esculenta have shown significant experimental activity that supports the dietary use of the plant for lowering blood cholesterol levels. This may explain the lower cholesterol levels of individuals in Papua New Guinea who incorporate Taro into their diet. 14 Glycerols (mono- and digalactosyldiacylglycerols) were identified as the active components. These compounds, which are also present in the green microalga Chlorella vulgaris, have shown anti-tumour promoting activity (Sakano 2005; Morimoto 1995). The low rate of colorectal cancer in Hawaii and New Zealand may be linked with the beneficial effects of poi (Colocasia esculenta starch) in the diet. Investigations have shown it had an anticancer (antiproliferative) activity against colon cancer cells, as well as a positive immunostimulant effect (Brown 2005; Ferguson1992). In addition, lignans and fatty acids from Colocasia antiquorum var. esculenta tuber bark have anti-melanogenic activity – that is, they act to inhibit the production of the pigment melanin. This suggests that these compounds may be useful against skin damage with cancerous (melanoma) potential (Kim 2010). Taro has had an interesting reputation as an antiinflammatory and nerve tonic in Indian medicine traditions, and is considered useful for the treatment of nervous disorders (emotional distress and depression). Recent studies of the neuropharmacological activity of Colocasia esculenta leaf extracts have shown anxiolytic, anti-depressant and mild sedative activity. This was 14 There are other tuber-based vegetables with similar potential. They include Arrowroot, Tapioca (cassava starch), Yams (Dioscorea alata, D. esculenta), Colocasia and Sweet potato (Ipomoea batatas). Studies in rats have shown these vegetables decreased tissue cholesterol and triglyceride levels in cholesterol-fed animals (Prema & Kurup 1979).
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possibly linked to the presence of flavonoids, steroids and β-sitosterol. A potent sedative activity has been exhibited by some steroidal agents, while flavonoids such as apigenin and luteolin (which are found in the leaf extract) have anxiolytic properties (Kalariya 2010).
• In addition to oxalate poisoning there are a number of other contact irritant toxins that can impact quite dramatically on human health. Those that contain resins with a corrosive characteristic would have to be among the most disconcerting and highly discomforting. While the joys of encountering the extremely irritant Blind-your-eye Mangrove have already been mentioned, there are other native and imported plants with equally distressing potential. In particular, dermatitis and allergic reactions from exposure to a number of the Anacardiaceae family can be quite hazardous – this includes the Cashew Nut, Australian Cashew, Mango and Poison Ivy. Encounters with some of the Ranunculaceae (Buttercup family) can be similarly painful. From a medical point of view, reactions to these plants are often not easy to deal with. The detoxification methods required to ensure that irritant exposures are avoided, thereby permitting the culinary use of a variety of resin-containing produce, is not simply linked to a ripening process or washing away the toxin. Intricate and involved processing techniques have had to be devised to enable the development of marketable products. Indeed, many of us would have little appreciation of the complexity involved in getting a simple Cashew nut into a packet and onto the supermarket shelf. Investigations of their medicinal value have inspired an equally surprising journey by modern research.
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The presence of caustic and corrosive agents in some plant families can present a significant problem for those who are unaware of the dangers of exposure. Individuals who are allergic to these plants face hazards that can be perilous in the extreme. The Anacardiaceae have a particular reputation for allergic reactions, which includes reactions to various fruits, nuts and, of course, the infamous Poison Ivy. The Buttercups (Ranunculaceae) are another classification that contains a highly irritant latex and little is known regarding the native species – although a few weedy imports have a serious reputation for caustic reactions. Fortunately, the acrid burning taste of most Ranunculus species generally acts as a deterrent to experimentation by both humans and stock. Selwyn Everist (1981) commented with regard to the native species that: ‘In the field, cases of buttercup poisoning are quite rare, despite the abundance of these plants in some seasons and in areas where sheep, cattle and horses have ready access to them. Most of them appear to be unpalatable and, even when they are eaten, conditions for the release of large amounts of protanemonin are often unfavourable.’ Even so, instances of severe gastrointestinal irritation, as well as fatalities, have been reported in animals grazing on plants such as Traveller’s Joy (Clematis vitalba)1, Lesser Celandine (Ranunculus ficaria), Meadow Buttercup (R. acris), Lesser Spearwort (R. flammula) and Celery-leaved Crowfoot (R. scleratus). However, stock feed contaminated with dried buttercups is harmless (Cooper & Johnson 1984; Turner 1984; Minakata 1983).
Corrosive Buttercups
Among the more familiar of the Ranunculus species found in Australia are the Meadow Buttercup (Ranunculus acris), the Celery-leaved Buttercup or Crowfoot (R. scleratus) and the Lesser Spearwort (R. flammula). Weedy species include the Corn Buttercup (R. arvensis), Australian Buttercup (R. lappaceus), Sharpfruited Buttercup (R. muricatus), Snake’stongue Buttercup (R. ophioglossifolius), Smallflowered Buttercups (R. parviflorus and R. sessiliflorus), Creeping Buttercup (R. repens) and the Large Annual Buttercup (R. trilobus). The vesicant (blistering) reputation of the genus is linked to a pale yellow oil that contains protoanemonin – a compound formed from glycosidic precursors in the plant (notably the toxic component ranunculin). Protoanemonin, albeit a powerful vesicant agent, has effective antibacterial, antifungal, antimutagenic and Ranunculus acris. (Courtesy: Serge Aubert, SAJF)
Ranunculus repens. (Courtesy: Rasbak, wiki)
1 Clematis also belongs to the Ranunculaceae, and there are 17 Clematis species (including C. vitalba) found in Australia, a number of which are native.
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anthelmintic activity. Protoanemonin, however, is highly unstable and is readily converted to a more inert derivative, anemonin – which is much less active, although it retains antibacterial properties. This also results in modification of the severity of the herbs’ vesicant properties which are apparent only on contact with the fresh plant. Heat exposure (cooking) is usually effective for detoxification of these herbs, although merely crushing or pounding will facilitate the process. This permitted the use of many European species of Ranunculus as pot herbs, although, at times, the strategy failed due to inadequate cooking: ‘some cases are reported where this happy result failed, and serious symptoms supervened’ (Millspaugh 1892). Poisoning from protoanemonin in animals and humans has similar symptoms: stomach pain, throat inflammation, salivation, cracked and excoriated tongue, smarting teeth, tenderness, and bleeding of the cornea of the eye (Millspaugh 1892). The protoanemonin content of Rancunculus
Ranunculus bulbosus, from Medicinal Plants. Charles F Millspaugh, John C Yorston & Co., Philadelphia,
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species can vary substantially, which explains their variable toxic reputation. Studies of various northern hemisphere species have shown high levels of ranunculin in R. bulbosus, R. flammula, R. gramineus, R. sardous and R. stevenii (Didry 1993). According to studies by Shearer in 1938, the early growth of Ranunculus bulbosus had one-sixth of the amount that was present during flowering. The level in Ranunculus sceleratus was 2.5 per cent when mature (just after flowering), while lesser amounts were present in the following species: 1.45 per cent in Ranunculus flammula, R. parviflorus, R. acris and R. bulbosus; while only 0.27 per cent was found in R. repens (Turner 1984). Studies of Ranunculus bulbosus have reported significant antimicrobial properties for protoanemonin (a lactone), particularly against various Streptococcus bacteria. It is of particular interest that the antimicrobial effect could be enhanced by combination with various conventional antibiotic drugs. This activity was linked to the ability of protoanemonin to penetrate the microbes’ cell walls, thereby facilitating the entry of the antibiotic, with a resultant enhancement of its efficacy (Didry 1993). Unfortunately an evaluation of Australian native species does not appear to have been undertaken. Therefore, we know virtually nothing with regard to the medicinal potential of these herbs. Anemone flower. Other Ranunculaceae genera with acrid, irritant properties due to ranunculin include Helleborus, Clematis and Anemone – which all contain herbs of medicinal interest. Some Anemone species have shown a wide range of pharmacological activities: amoebicidal, antibacterial, antifungal, analgesic, hypotensive, sedative and antispasmodic.
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A good deal of confusion has existed with regard to the Ranunculus species responsible for incidents of poisoning: ‘Most of the references to toxicity in Australian species appear to be based on conjecture or confusion of identity with overseas species of known toxicity. It has been difficult or impossible to find definite reports of poisoning for several of the Australian species commonly cited as being toxic’ (Everist 1981). The situation does not appear to have changed much over the decades, with little interest being expressed in any review of the toxicology of the native plants. It leaves one wondering at their poisonous and medicinal potential, considering that there are at least 55 species found in Australia – this includes a few weedy naturalised species, some of which have a traditional medicinal reputation.
Toxic Bush Tucker
The presence of a ‘Cashew nut’ was one of the early discoveries of Captain Cook’s Endeavour voyage to Australia. On 24 July 1770, Joseph Banks wrote of his frustration at collecting botanical samples during an exploratory survey at the Endeavour River in northern Queensland: The blowing weather which had hindered us from getting out several days still lasted, not at all to our satisfaction who had not one wish to remain longer in the place, which we had pretty well exhausted even of its natural history. The Dr. and me were obliged to go very far for anything new; to day we went several miles to a high hill where after sweating and broiling among the woods till night we were obliged to return almost empty. But the most vexatious accident imaginable befel us likewise: traveling in a deep vally, the sides of which were steep almost as a wall but coverd with trees and plenty of Brush wood, we found marking nuts (Anacardium orientale) [= Semecarpus australiensis] laying on the ground, as desirous as we were to find the tree on which they had grown, a thing that I believe no European Botanist has seen, we were not with all our pains able to find it; so after cutting down 4 or 5 trees and spending much time were obliged to give over our hopes.
Banks’ frustration at being unable to find his botanical specimen has been echoed by many rainforest botanists over the intervening centuries. Rainforest trees are in general extremely tall, vanishing into the canopy high
Grassy Hill, Cooktown. In 1770, this is the viewpoint from which James Cook and some of his crew would have seen the surrounding countryside. Cook’s journal reveals some dismay at the options presented to him during his enforced stay at the site while he was undertaking repairs to HMB Endeavour: ‘This afternoon I went upon one of the highest hills over the harbour from which I had a perfect View of the inlet or River and adjacent country which afforded but a very indifferent prospect.’ From here he could also obtain a good view of the reef enabling him to make decisions regarding the best course to continue his voyage. Almost two weeks later he returned to this vantage point to reassess the situation: ‘I likewise sent some of the young gentlemen to take a Plan of the harbour and went myself upon a hill which lies over the south point to take a view of the Sea, at this time it was low-water, and I saw what gave me no small uneasiness which were a number of Sand banks or shoals lying all along the coast … The only hopes of geting [sic] clear of them is to the northward.’ (Image courtesy: Mark Maupin)
above. This easily conceals the origins of their fruit, making the source unrecognisable. The steep inclines of the terrain would help to obscure the site of the parent tree, which would not be readily apparent from the location of the fruit on the ground. The thick jungle vegetation, often obstructed by sharp-hooked Lawyer cane vines, can be virtually impenetrable.
The jagged rocks found along the northern coastline are a serious obstacle for mariners.
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and even acute dermatitis. The husk or shell likewise produces a contact dermatitis. The tar from the bark is also vesicant.’ These symptoms are virtually identical to reactions reported from exposure to the latex of the Australian Cashew, Semecarpus australiensis.
Queensland Tar Tree, Semecarpus australiensis.
The fleshy part (the pedicel) of the fruit of the Australian Cashew (Semecarpus australiensis) is a thickened stem, which is attached to the nut. Although edible, the fruit must be ripe and the skin peeled off before use – ensuring that any latex remnants will be completely removed. To be perfectly safe, it is probably wise to adopt the same cooking practices as Aboriginal people, who also roasted the pedicel (Jackes 1992; Everist 1981).
Cashew – A Famous Relative The genus Anacardium is closely related to Semecarpus, with very similar properties, both toxic and medicinal, with the fruit (particularly the nuit shell) retaining a substantial amount of irritant resin. Watt and Breyer-Brandwijk (1962) note: ‘Although the seed kernel of Anacardium occidentale is edible, it is actually poisonous unless roasted until all the pericarp oil has exuded. The fumes which come off during the process are highly irritant. The oily juice is dark brown, almost black, in colour, extremely acrid and irritant to the skin: causes swelling, rubefaction, vesication,
The tropical Queensland Tar Tree or Australian Cashew, Semecarpus australiensis, occurs from Cairns to Cape York, extending to the islands of the Torres Strait. Dr Hugo Flecker commented: ‘The “tar tree” is a very large, handsome tree, native to North Queensland, with deep green leaves providing an abundant shade and formerly was plentiful about
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Anacardium occidentale, from Kohler’s Medicinal Plants, 1887. The fruit of the Cashew (Anacardium occidentale) and the Australian Tar Tree (Semecarpus australiensis) have a somewhat odd appearance because a fleshy pedicel sits over the top of an exposed seed-containing nut below. While the nut of the normal Cashew is kidney-shaped, that of the Australian Cashew has a more oval appearance.
Cairns, but owing to its unmerited reputation as a source of irritation, its numbers in recent years have unfortunately been greatly reduced’ (Flecker 1945). Many would disagree with his use of the term ‘unmerited’ – the tree has retained its poisonous fame, and with some justification. In 1847 Ludwig Leichhardt wrote of a painful and discomforting encounter at Port Essington: ‘we also found a new tree, a species of Anacardium [= Semecarpus australiensis], which the natives called “Lugula”; it bore a red succulent fruit, formed by the enlargement of the stalk, with [a] greyish one-seeded nut outside, like Exocarpus. The fruit was extremely refreshing, the envelope, however, contained such an acrid juice that it ate into and discoloured my skin, and raised blisters wherever it touched it: these blisters were not only followed by simple excoriation, but by a deep and painful ulceration.’ Overseas, other species of the Semecarpus genus have a similar reputation.
The fruit of the Australian Cashew tree is not designed for casual tasting experiments and, while Aboriginal people ate the roasted nut, it was first subjected to processing. In a paper on the toxic components of the nut, PB Oelrichs (1997) commented: ‘Native cashew (Semecarpus australiensis) is a well-known food source for Aboriginal people of northeastern Queensland and the Northern Territory. It is also well known that contact with the seeds at a certain stage of growth can cause severe dermatitis in susceptible individuals. To prepare the fruits for eating, they are commonly treated by leaching for 2–7 days with water followed by heating in bark, and this treatment apparently produces an edible cashew nut.’ Unroasted, the nut would have serious side-effects if eaten, resulting in particularly severe swelling and burning of the lips and the mucous membranes of the mouth. As a protective strategy Aboriginal women coated their hands with clay whenever preparing the fruit – then washed their hands thoroughly before touching anything else, or any person. Children were actively discouraged from climbing the tree. Mere scratches could become inflamed and fester. Even the smoke from the wood on a cooking fire has been reputed to cause skin reactions. The Cashew tree itself (Anacardium occidentale), which contains closely allied compounds, has a similar reputation, as Eduardo Quisumbing (1951) commented: ‘The Filipinos are very careful when they roast the seeds. The fumes which rise when the nuts are heated should not be allowed to reach the face or eyes as they are very irritating. They also cause irritation in the nostrils and throat.’ While the Cashew’s irritant component (urushiol) is not volatile, the smoke can carry it on dust particles, somewhat unexpectedly facilitating wider contact with the allergen (Barceloux 2008).
The Anacardiaceae Family: Irritants and Allergens The resin of the Australian Cashew tree (Semecarpus australiensis) has a tarry character that is unmistakable: ‘The seeds sometimes drip a dark-coloured oily resin which hardens into a black, lacquer-like coating on objects left standing under the trees. Contact with this resin can produce severe dermatitis in susceptible
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In the seventh edition (1949) of his Manual of Pharmacology, Torald Sollmann mentioned the irritant properties of these plants: Anacardium (active principle, cardol, an oily substance); Semecarpus, a variety of ornamental woods, especially tropical but also domestic, with marked difference of susceptibility [to cause dermatitis] … The sap of a variety of tropical plants of the Anacardiaceae, including the mango, produces allergic dermatitis, probably by an identical or related substance … ‘Dhobie’ dermatitis in East India results from contact with linen marked by native launderers with a fluid from the fruit of Semecarpus Anacardium … The latex of Semecarpus atra, the ‘acajou’ tree of South Pacific islands, produces severe dermatitis; the natives believe that this may occur from sleeping under the tree.
Australian Cashew Nut showing resin-coated fruit and resin-impregnated tree bark.
people’ (Everist 1981). The sawdust was the cause of similar discomfort. The term ‘Marking Nut’, which is often applied to the fruit, originated from the use of an ink prepared from the resin of various Semecarpus species, notably the Asian Semecarpus anacardium. It has indelible waterproof marking properties, particularly useful for marking laundry, although the use of alcohol could cause it to fade. The milky juice of the Poison Sumach (Rhus vernix), which has similar vesicant attributes, was an equally useful marker for linen2 (Le Strange 1977) – as was the milky juice of the Cashew tree
(Anacardium occidentale).
A transparent irritant oil (urushiol), which is found within the tree’s tissues3, polymerises into a shiny, black lacquer4 when exposed to oxygen – a process that takes around 24 hours. This reduces its potency, although it does not entirely eliminate its allergic potential. Urushiol, which is very adherant, can even penetrate rubber gloves because the component catechols are soluble in rubber. This can pose a serious potential problem for allergic individuals who are unaware of the risk. Despite the fact that washing will remove the resin from the skin and clothes, once skin contact has been made the allergic reaction can proceed in sensitive individuals regardless of attempts to remove the offending agent. However, there is usually a timelag due to a delay in the urushiol compounds binding to the skin (30–60 minutes) and washing with soap (alkaline soap, dishwashing liquid) can modify the intensity of the reaction (Barceloux 2008). It is important to note that the substance itself is not the problem – it is the body’s reaction to the allergen. Thus individual differences in tolerance and recognition of the allergic substance come into play in determining the severity of the reaction. 2 Rhus vernix had another interesting use, the resin being added to liquid leather dressings (or varnish-like polishes) for finishing shoes and boots (Le Strange 1977). 3 The oily liquid urushiol, which is also found in the nut shell, is the primary allergen. It is composed of phenolic compounds that include anacardic acids (urushiols), as well as cardol, which is toxic, and its derivative cardanol, which is not (Phani Kumar 2002). 4 In the Moluccas the resin of Semecarpus cassuvium was formerly used by the Amboinese as a varnish for shields, spear handles and walking sticks (Burkill 1935).
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Urushiol, which is widespread in the Anacardiaceae,
belongs to a class of compounds (catechols) that is responsible for the toxic properties of many species in this family – although the concentration of catechols can differ between species, and even between individual plants (Barceloux 2008). Urushiols that have been isolated from Semecarpus australiensis are
similar to those found in Poison Ivy (Toxicodendron radicans), another member of the Anacardiaceae – although the yield from the Native Cashew was noted to be ‘considerably higher’ (Oelrichs 1997). For purposes of commercial exploitation the removal or conversion of the toxic components from the nut is essential, while concurrently retaining the attractive flavour of this Australian bush food, which has been compared to that of the Brazilian Cashew (Anacardium occidentale).
Ivy Dermatitis
Ivy, Hedera helix, on tombstone and statue. The nut shell of the Australian Cashew (Semecarpus australiensis) has a double-layered design, very similar to that of the Brazilian Cashew. It consists of an outer shell (epicarp) and a tight-fitting inner shell (endocarp) surrounding the nut within. Sandwiched between the two outer layers is a honeycomb-structured filling that contains a caustic oily sap (the nut shell liquid). The Australian Cashew, which has crop potential similar to the Cashew, requires detoxification before it can be considered suitable for the marketplace – a process that needs to neutralise the irritant activity of the nut shell liquid without detracting from the flavour of the nut itself (Oelrichs 1997).
Dermatitis due to Ivy (Hedera helix) should be differentiated from that of Toxicodendron (or Rhus) Poison Ivy. Hedera helix is a commonly cultivated European vine with substantial weedy potential that has become widespread throughout the world. The vine can cause a delayed hypersensitivity reaction that results in a vesicant form of eczema – particularly in individuals such as gardeners who have become sensitised to the plant. Ivy stems and roots contain fairly high levels of falcarinol – a
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Table 6.1 Common toxic trees of the Anacardiaceae that contain urushiol components Species (common name)
Distribution
Anacardium occidentale Cashew tree
Tropical America. Cultivated worldwide. Australia: naturalised in Queensland and Northern Territory (NT).
Mangifera indica Mango tree
Southern Asia (notably eastern India, Burma, Andaman Islands). Cultivated throughout the tropics. Australia: naturalised in the tropics.
Pistacia vera Pistachio tree
West Asia, Asia Minor (Turkey, Afghanistan).
Semecarpus anacardium Indian Marking Nut tree
India, Southeast Asia, Pacific Islands.
Australia (tropical regions): NT, northern Queensland (incl. Cape York). Semecarpus australianum Australian Marking Nut; Australian or Native Cashew Schinus molle (syn. S. areira) Peruvian Pepper tree
South America, Mexico: widely cultivated for use as a pepper-spice (pink peppercorns). Problematic weed: regarded as a serious international weed. Australia: naturalised in Queensland, Northern Territory (NT), New South Wales (NSW), Western Australia (WA); widely considered to be an invasive weed.
Schinus terebinthifolius Brazilian Pepper tree; Florida Holly
South America (tropical and subtropical regions): widely cultivated for use as a pepper-spice (pink peppercorns). Problematic weed: Florida and Hawaii (invasive weed). Africa (invasive weed). Australia: naturalised Queensland, NT, NSW, WA: considered to be an invasive weed.
Toxicodendron succedaneum Japanese Wax tree, Scarlet Rhus
Japan, Asia: widely cultivated ornamental. Australia: listed as a pestilential weed in ACT, NSW (declared plant), South Australia (proclaimed plant), Queensland (naturalised).
Toxicodendron verniciflua Japanese Lacquer tree
Japan and China
Toxicodendron radicans Poison Ivy and related Toxicodendron (Rhus) species
North America (Canada, USA, northern Mexico). Australia: T. radicans: South Australia (proclaimed plant), Queensland (naturalised). T. diversilobum (Western Poison Oak): Queensland (naturalised).
Ivy Dermatitis (continued) compound with moderate allergic potential that is not chemically related to urushiol. Falcarinol is also present in the Carrot family (Apiaceae) and may contribute to allergic reactions, although these plants also contain photosensitising agents (furocoumarin compounds) that are activated on light exposure, giving reactions that resemble sunburn (Barceloux 2008; Ozdemir 2003).
Hedera helix
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Urushiol
Urushiol components (notably anacardic acids) are not limited to the Cashew Tree as they are fairly widespread in the Anacardiaceae – for example, they are present in Anacardium spondias and Spondias mombin (Coates 1994; Gellerman 1976). Somewhat surprisingly, they have also been found in the Gingko or Maidenhair tree, Ginkgo biloba (fruit, seeds, leaves), illustrated here. Despite the fact that it belongs to a completely different family (Ginkgoaceae), the fruit has an irritant reputation, similar to that of the Cashew, due to allergenic urushiol components (specifically, ginkgolic acids). However, once the herb is processed only minute amounts are present (below the detection limit of 0.03 ppm) – an analysis that supports the efficacy of the techniques utilised for detoxification. Interestingly, although Ginkgo also contains cardanols, these compounds were not implicated in studies of allergic dermatitis reactions to the plant (Schötz 2004, 2002).
The Pistachio Tree (Pistacia vera)
Pistachio nut.
The Pistachio tree (Pistacia vera) is a famous medicinal and culinary plant in the Anacardiaceae. This small tree is native to West Asia and the Levant (Turkey– Afghanistan region). Records relating to the use of the nut in antiquity date back at least to 7000 BC.
Pistacia vera, from Kohler’s Medicinal Plants, 1887.
The colour of the nut kernel is chlorophyll-based, and it imparts a green hue to culinary items such as bakery products. Nuts of a darker green were highly prized. Traditionally, the Pistachio tree has been used as a remedy for abdominal, chest and circulatory disorders, as well as liver sclerosis (hardening of the liver). It has been utilised for rheumatic pain, traumatic injuries, bruising and sores. In addition, the Reverend GA Stuart noted in his 1911 work Chinese Materia Medica: ‘This is of foreign origin … The kernels of the nuts are said to be good for dysentery, and to be very nutritious, promoting the growth of flesh. The bark of the tree is said to be strengthening to the female principle, and is used in decoction in pruritus [itching] of the genitals.’ The closely related resin-yielding Mastic Tree (Pistacia lentiscus) had a more extensive medicinal reputation, primarily as an analgesic and sedative, for treating gastric disorders (gastralgia, peptic ulcers), cardiac pain, gynaecological problems (e.g. amenorrhoea, mastitis), and as an expectorant and antitussive in respiratory tract disorders (Duke & Ayensu 1986; Keyes 1975).
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Indian Marking Nut (Semecarpus anacardium)
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A Complex Detoxification Process
The Marking Nut tree (Semecarpus anacardium) has been widely cultivated in places as far afield as Mauritius, East Africa and China, with the apple-flavoured fruit pedicel often found in the local markets. (Image courtesy: H Zell, Wikipedia)
Semecarpus anacardium, from William Roxburgh and Sir Joseph Banks, Plants of the Coast of Coromandel, Vol. 1, 1795.
Throughout Southeast Asia and the Pacific Islands the genus Semecarpus is known to cause irritant skin reactions, although the toxicity appears to vary between species. Among the most poisonous are the Javanese Semecarpus heterophylla and the Philippine Ligas tree, Semecarpus cuneiformis. Even rainwater dripping off the latter can cause skin irritation. The smoke of the burning branches is also toxic. The sap of the Ligas causes a typical, and highly painful, skin vesication (swelling and blistering); it has, however, been used in the treatment of ‘indolent’ ulcers. Henry Burkill (1935) commented that Semecarpus cassuvium (from the Moluccas) had similar uses, with equal potential for discomfort: ‘On tender skins it is a cure of a rather heroic nature.’ Burkill regarded Semecarpus heterophylla as being the most poisonous of the genus: ‘if it [the resin] falls on the skin it causes an itch and swelling which may fester and [be] got to heal only with some difficulty’.
Many plants that have been utilised in classic Indian herbal medicine traditions (Ayurveda, Siddha, Unani) have poisonous properties. This inspired the development of sophisticated, and sometimes complex, processing methods to reduce their toxicity. Henry Burkill (1935) provides an interesting description of the extensive processing to which the seeds of a Semecarpus species from the Andaman Islands were exposed: • The fruit wall was removed and the seeds cleaned, then wrapped in leafy bundles and parboiled. • Fermentation followed when the seeds were buried in the earth for several weeks. • Eventually they were unearthed and dried, after which they were baked before being deemed edible. Other detoxification practices were equally labourintensive. One complex recipe combined the kernels and crushed seeds of the Indian Marking Nut marinated in cow’s urine overnight for three days. Each day they were removed from the mix and sundried. Eventually they were decocted with Myrobalan (Terminalia bellirica) roots, followed by boiling in a buffalo-dung solution – after which they were dried again and finally washed in rice water (Patwardhan 1988). The extract was traditionally administered with peanut oil. The whole process appears to have been effective as tests have verified the safety of the result, although no comment was made regarding the palatability of the end product (Shanavaskhan 1997).
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of Ayurvedic Medicinal Plants, comments: ‘The juice of the shell of the nut is a powerful escharotic; given in small doses with oil or butter in leprous and scrofulous affections, syphilis, skin diseases, epilepsy, nervous debility, neuralgia, asthma, dyspepsia and piles. The bruised nut [is] used as abortifacient by placing it in the mouth of the uterus; also given as a vermifuge.’ The brownish gum exudate from the bark was applied to scrofulous, venereal and leprous afflictions, as well as being recommended for nervous debility, and as an effective cardiac tonic (Kapoor 1990). There have been some unusual recommendations associated with the Indian Marking Nut (Semecarpus anacardium). One involves its use as a worm-killing medicine for elephants. Per elephant, fifty Indian Marking Nut seeds were ground with Datura metel fruit, and salt. The animals, who present with symptoms of diarrhoea, indigestion and eating soil, are treated with a single dose of the medicine in their fodder (Singh 1996). (Image courtesy: Winsome Cupitt)
Over a century ago, the eminent Australian botanist Joseph Maiden (1889) mentioned the use of the Indian Marking Nut tree for destroying warts, removing ‘scrofulous’ eruptions and for treating sprains or rheumatic problems in Indian traditions. It was, at times, even employed for purposes of misrepresentation by inducing deliberate injury: ‘The nut is also used to produce the appearance of a bruise in support of criminal charges preferred through enmity, its application in a diluted form producing great oedematous swelling and redness of the skin. It is also used as a fumigation for haemorrhoids in India; it causes sloughing of the tumours. It is given internally in asthma, after being steeped in buttermilk, and is also given as a vermifuge. Both the nut and the oil obtained from it are used in India for purposes too numerous to mention.’ Indeed, a paste prepared from the root mixed with potash has even been applied externally as a traditional antidote to snakebite in northern India. The plant has retained its therapeutic reputation in Ayurvedic medicine. The ripe fruit is regarded as having acrid, stimulant, digestive, sedative, antispasmodic, alterative, nervine tonic and escharotic (corrosive or caustic) properties.5 LD Kapoor, in the CRC Handbook 5 In addition, fruit extracts of Semecarpus anacardium have shown male anti-fertility effects – acting to inhibit spermatogenesis, as well as causing a substantial reduction in sperm density and motility (Sharma 2003).
Poison Ivy: An Infamous Vesicant
Toxicodendron diversilobum, Poison Oak. (Courtesy: Fell Wraith, Wikimedia Commons)
The overt toxicity associated with unprocessed Cashew oils and sap can be linked to allergic reactions involving other plants within the Anacardiaceae family. Individuals who are particularly sensitive run a high risk of allergic reactions with severe and dramatic potential. Contact allergens (urushiols) are present in the Poison Ivy (Toxicodendron radicans, formerly Rhus radicans or R. toxicodendron)6 and related 6 While the term ‘ivy’ conjures up images of a creeping vine-like plant, Poison Ivy can also take the form of a sprawing vine or a shrub. Indeed, older specimens growing on good support structures can reach proportions that allow them to be mistaken for a tree. The plant has a wide tolerance of environmental conditions ranging from woodlands, waste sites and urban environments, to exposed rocky sites.
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species such as Pacific or Western Poison Oak (R. diversilobum), the Poison Sumach or Poison Elder (R. vernix) and the Fragrant Sumac (R. aromatica). Slight contact with undamaged leaves may not cause any problem, as it requires a form of tissue injury for the plant to release the oil. However, the leaves have usually been damaged in some way, allowing easy contact with the urushiol oil within. Because it degrades very slowly the allergen may be present even in dead leaves (see www.kingdomPlantae.net). Reactions can also be influenced by the amount that is present. Most of the year the level in Poison Oak leaves is low (0.02–0.04%), although in early November the urushiol content increases substantially (0.9–2.6%) when they turn red and become brittle. By December, when the leaves fall, the allergen component is low and the leaves are no longer allergenic. However, during the winter, the sap in the twigs of the Poison Oak and Poison Ivy contain a significant urushiol component (Barceloux 2008; Gartner 1993). The irritating discomfort can involve various levels of dermatitis that can result in severe blistering. Those sensitive to Poison Ivy can also develop skin sensitivity to Cashew shell oil.7 Dockworkers in Europe once suffered a skin condition called ‘vanilla itch’. This was attributed to a Cashew extract that was painted on Vanilla pods to give them a bright shiny finish. The Pistachio nut contains similar allergens. The effects of urushiol can be highly distressing: Contact with certain species of Rhus, common along roadsides, on fences, in woods and swamps, produces dermatitis (Captain John Smith, 1609) passing through hyperemia and itching to violent vesication, edema and suppuration, according to the specific sensibility of the individual. Many persons are practically immune, although a sufficient quantity of the isolated principle has never failed to produce the dermatitis. It is believed that the dermatitis is an anaphylactic phenomenon requiring sensitization by previous exposure. The susceptibility probably diminishes in time if it is not maintained by repeated exposure. It 7 There is, however, an interesting report that mentioned reduced sensitisation to Poison Ivy in staff working with Cashew shell nut oil over a long period (Reginella 1989).
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does not produce bronchial or other anaphylactic symptoms. The active ingredient of all the species, urushiol, a mixture of closely related catechol derivatives, occurs as a resinous oil, contained in the sticky sap of the plants, which exudes when the plant is injured. It becomes inactivated by oxidation through laccase, a polyphenolase occurring in the sap of these plants... it is so highly active that 1/1000 mg. has caused severe vesication … It is not volatile, but it may be carried to some distance on the soot in the smoke of burning plants, and perhaps on dust … and by some insect alighting on injured plant. None is present in the pollen … It may be conveyed by the hands or clothing from one person to another, as if it were contagious (Sollmann 1949).
The fact that the development of symptoms can often be latent easily complicates the diagnosis. Irritant symptoms may appear anywhere from 1–9 days (usually 4–5 days) following exposure, and then take another 4–6 days to subside.
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Toxicodendron diversilobum, T. radicans (illustrated here) and T. succedaneum are naturalised in Queensland, with the latter found also in New South Wales. Poison Ivy is difficult to eradicate, and the cure can be far worse environmentally than the problem plant, particularly if pesticides are employed. The plants are best dug out of a site, although they may well grow back, and persistence is required. Burning them will only result in widespread distress as it allows the allergen to spread on the smoke. (Image courtesy: H Zell, Wikimedia Commons)
Chinese Lacquer
The use of natural resins as a lacquer (a clear form of varnish) is an ancient art. However, some resins can have significant allergic potential. The Chinese Lacquer Tree (Toxicodendron
Th of ca L sy kn la an oi on Th co u to w va in ca is le u re M tr b in [b
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vernicifluum, syn. Rhus verniciflua), which is among the best known of these resin-yielding trees, contains large amounts of urushiol, a polysaccharide and the enzyme laccase. This naturally occurring oilin-water emulsion will solidify (polymerise) on Lacquer bowls with goldfish motif. (Courtesy: exposure to air in warm humid conditions. The GiftsbyGloria) lacquer is a prized hard, durable, waterproof coating that can take on any form of sheen, albeit usually employed as a high gloss finish. The toxic properties of the sap are greatly reduced with drying, although during processing the vapour retains its aggravating attributes. Some individuals find that even handling lacquerware can be responsible for allergic reactions unless it is heat treated – a process that renders the product less allergenic because it substantially reduces the urushiol component of the lacquer (Kawai 1992). Rhus verniciflua has also acquired a medicinal reputation, which is outlined in the Chinese Materia Medica of Reverend GA Stuart: ‘[The] juice of the tree dessicated and pulverized. It is considered to be tonic and stimulant, and is prescribed in coughs, intestinal worms, amenorrhoea, and ecchymoses [bruising]. The leaves are used in wasting diseases and intestinal parasites, the seed in dysentery, and the flowers in the swelled belly of children’ (Stuart 1911). However, systemic reactions can occur in individuals who are sensitive to Rhus lacquer. Symptoms involve not only the development of skin lesions (redness, swelling, pustules, purpura, weals, blisters, itching), but also gastrointestinal problems, fever and chills, as well as immune system stimulation (leucocytosis, neutrophilia). Severe reactions can involve damage to kidney and liver function (Park 2000; Oh 2003). In Korea a traditional remedy for gastrointestinal disorders is prepared from boiled chicken with Rhus lacquer – a ‘health food’ that has been responsible for some serious allergic reactions as
the cooking process does not completely detoxify the urushiol components (Cheong 2010). There is evidence that lacquer craftworkers can develop a level of tolerance, with diminished reactivity (hyposensitisation) leading to a reduced incidence of dermatitis. Even so, there will always be the unfortunate few who will not be able to tolerate the product at all (Kawai 1991).
New Discoveries from a Traditional Medicinal Plant
The close botanical affinity between the Australian Cashew (Semecarpus australiensis) and the Indian Marking Nut (Semecarpus anacardium) as well as their similar toxic properties, has led to speculation with regard to their medicinal activity. Few studies have been done using the Australian Cashew and its pharmacological merits must largely remain a matter of conjecture at this point. However, the continued traditional use of the Indian Marking Nut has fostered substantial research into the pharmaceutical value of this species that have revealed some very interesting potential. Indian Marking Nut extracts possess significant antimicrobial attributes, including activity against various Clostridium bacteria – the agent responsible for conditions such as tetanus. In particular, the compounds bhilawanol A1 and B2 have shown inhibitory effects against Clostridium tetani (Nagabhushana 2002; Lamture 1982, Patwardhan 1982). Infection with this bacterium can result in nerve paralysis as it produces a potent neurotoxin, although this is only formed within the body or when injected. This is why puncture wounds from items such as a rusty nail or dirty rose thorn can be extremely dangerous. When Clostridium tetani is ingested it is harmless, as the bacterium is detoxified by the digestive process.
An Anticancer Reputation
In Siddha medicine the Indian Marking Nut (powdered, with the oil removed) has been made into pills with palm jaggery for use as an anticancer drug. The nut milk (the nut infused in milk) has a similar use. Another commonly utilised anticancer remedy involves a combination of Semecarpus anacardium (fruit), Amoora rohituka (stem bark)
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and Liquorice (Glycyrrhiza glabra) roots. These preparations have achieved a good reputation for effectiveness. Indeed, studies have clearly demonstrated anticancer properties for the nut. The Indian Marking Nut can act to induce apoptosis (programmed cell death), a strategy designed to induce cancer cells to self-destruct. Extracts have shown promising potential for the treatment of a range of cancers (oesophagus, urinary bladder, liver, breast) – as well as leukaemia (Nair 2009; Verma & Vinayak 2009; Sugapriya 2008; Sujatha 2002; Thatte 2000; Smit 1995; Indap 1983; Phatak 1983; Ghosh 1981). Indian researchers have invested a substantial amount of effort in investigations into the usefulness of the herb for mammary cancer. A popular Siddha herbal remedy for breast cancer, Semecarpus Lehyam, has been in use in southern India. It is based on a combination of six herbs – Semecarpus anacardium, Strychnos nux vomica, Strychnos potatorum, Smilax chinensis, Plumbago zeylanica and Nigella sativa. Experimental investigations have shown good results as an anticancer agent and identified catechols (urushiols) as the active components (Zhao 2009; Sowmyalakshmi 2005). Another combination remedy called Kalpaamruthaa (incorporating Semecarpus anacardium, Emblica officinalis and honey) has likewise shown significant cancer protective activity in animal studies. It would appear to have excellent potential – although this remains to be confirmed by clinical studies (Nair 2009; Mathivadhani 2006, 2007a, 2007b, 2007c; Veena 2007; Arulkumaran 2007, 2006; Arathi & Sachdanandam 2003). Investigations of the activity of Marking Nut on aflatoxin-induced liver cancer have shown reduced hepatotoxicity, with flavonoids identified as the active components. This has led to suggestions for the use of the drug in hepatocarcinoma (Premalatha & Sachdanandam 1999a; Premalatha 1997). Further investigations have been undertaken to explain its biological mechanisms, with clinical studies supporting its safety (Vijayalakshmi 2000; Premalatha & Sachdanandam 1999a, 1999b, 1999c, 2000a, 2000b, 2000c; Premalatha 1999).
Cardiovascular Benefits
The risk of cardiovascular disease becomes a matter of increasing concern with advancing age. The deposition of cholesterol in the blood vessels results
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in the formation of plaque that can eventually clog the arteries. This consequently reduces blood flow and increases the risk of a heart attack or stroke. The Marking Nut has shown substantial benefits for cardiovascular function with excellent clinical potential. The nut shell extract has been linked to significant reductions in cholesterol levels, notably LDL-cholesterol. It could prevent cholesterol deposition in various organs (liver, heart muscle, aorta), as well as inducing the regression of atheroma (fatty plaques). Additionally, Marking Nut extracts prevented cholesterol absorption, promoting its excretion from the gastrointestinal tract (Sharma 1995). Recent studies have also indicated nut extracts had direct cardioprotective attributes in combination with the widely used drug propranolol (Inderal). The latter is an antihypertensive agent that can help to relieve anxiety and panic states. In this study the combination had a protective action against the side-effects of isoproterenol (isoprenaline), which can cause increased heart rate (tachycardia) that may predispose to heart arrhythmia (Chakraborty & Asdaq 2011). This suggests that the herbal remedy has significnt clinical potential. Diabetic individuals may benefit from the use of Marking Nut extract as the remedy not only reduced cholesterol levels, it also helped to regulate blood sugar levels and protect against damage due to oxidative stress and cellular fatigue (Aseervatham 2011; Jaya 2010a, 2010b; Kathai 2005; Arul 2004). Cashew (Anacardium occidentale) seed, bark and root extracts and various components (including anacardic acid) have also shown anti-diabetic potential that could be of interest for the functional food market (Tedong 2010; Egwin 2005; Alexander-Lindo 2004). Compounds called cashew globulins were found to have similar cholesterol-lowering properties and could promote bile acid synthesis and excretion (Prabha & Rajamohan 1998). Ayurvedic formulations provide the benefit of complex, tried and tested herbal preparations that act synergistically. For instance, Semecarpus anacardium can be combined with a number of other respected medicinal herbs for use in cardiovascular complaints: Indian Guggulu or Gum-guggal (Commiphora mukul), Garlic (Allium sativum), Indian Plumbago (Plumbago indica), Hemidesmus indicus, Arjuna (Terminalia arjuna), Tinospora cordifolia, Sacred Basil (Ocimum sanctum) and Withania (Withania somnifera) (Mary 2003). Many of these herbal components have
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adaptogenic, antioxidant, anti-inflammatory and antibacterial attributes. The resultant cardioactive remedies not only possess an anti-atherogenic effect, they often incorporate a significant anti-inflammatory and tonic component.
Pain-relief and Anti-inflammatory Effects
Indian Marking Nut has achieved high esteem as an antiarthritic remedy. Numerous studies have confirmed that extracts have significant anti-inflammatory, analgesic, anti-oxidant and anti-arthritic activity (Lingaraju 2011; Singh 2006; Vijayalakshmi 1997, 1996; Patwardhan 1990; Saraf 1989). The remedy also appears to have potential as an anti-ulcer agent. Some studies have indicated that the anti-inflammatory activity is equivalent to that of conventional drugs such as indomethacin and ibuprofen. Tannins (polyphenolic compounds – notably bhilawanols and anacardoside a), numerous bioflavonoids (e.g. semecarpetin, semecarpuflavanone), and a range of vitamins and minerals have been listed among the active components8 (Tripathi 2010; Mythilypriya 2007b; Ramprasath 2004; Selvan 2004; Selvam & Jachak 2004). In addition, a bioflavonoid compound (THA: tetrahydroamentoflavone) from Semecarpus anacardium, which can be used as a marker substance for authentication of the herb, has shown significant xanthine oxidase inhibitory effects, suggesting its potential as an anti-gout agent (Arimboor 2010; Aravind 2008). Other research has indicated neuroprotective and memory-supportive potential for Semecarpus anacardium. Similar potential has been exhibited by cardanol derivatives from the Cashew Tree (Anacardium occidentale) – and by mangiferin, which is present in high levels in the Mango Tree (Mangifera indica), the African Honeybush (Cyclopia genistioides) and the Chinese herb Anemarrhena asphodeloides (Darvesh 2010; Jung 2009; De Lima 2008; Vinutha 2007; Bhatnagar 2005). A clinical study of the use of Semecarpus anacardium in 25 patients with rheumatoid arthritis has shown a complete remission in 40 per cent of the patients, while another 20 per cent had minor 8 The components vary according to the type of processing to which the remedy is exposed. In Ayurvedic traditions, the nuts are used after detoxification (heating), which would remove most of the irritant oil from the raw material. However, in Siddha medical traditions the whole nut is infused in milk, although it is used at very low dose (Tripathi 2010). (see: A complex detoxification process, page 207).
Rheumatoid arthritis is a distressing hereditary disorder characterised by inflammatory and destructive degenerative changes in the joints that may result in severe deformities and nodules. Equally distressing are the inflammatory effects that affect other systems, including the lung, heart, kidney and sclera of the eye. Complications include extreme fatigue, neurological damage, blood disorders (usually anaemia) and liver dysfunction. Not only is the condition extraordinarily painful, it is very difficult to treat. Rheumatoid arthritis is considered to be an autoimmune disease involving an abnormal immune response. Any remedies that can help, or minimise drug side-effects, would surely be a blessing. (Image courtesy: Bernd Brägelmann and Dr Martin Steinhoff, CCA-3.0)
improvements. Symptoms of body ache, general malaise and weakness were alleviated. There was also improvement in the appetite and digestive processes, as well as haemoglobin values. Some studies have suggested that the nut decoction (boiled) was more effective than cortisone (Upadhyay 1986). Kalpaamruthaa has shown similar clinical potential. Studies have confirmed that the formulation has significant anti-inflammatory, analgesic (antinociceptive), immunomodulatory and anti-arthritic activity, with substantial protective effects on joint tissue. It has also shown antipyretic potential and anti-ulcerogenic properties (Mythilypriya 2009, 2008a, 2008b, 2008c, 2007a, 2007b; Singh 2006; Ramprasath 2006a, 2006b, 2006c, 2006d, 2005a, 2005b). The antioxidant and anti-inflammatory action of a similar Ayurvedic herbal complex known as Sandhika have likewise been confirmed experimentally. The remedy is composed of Semecarpus anacardium and three other traditional anti-inflammatory, antiarthritic herbs – Commiphora mukul, Boswellia serrata and Strychnos nux-vomica (Tripathi 2009, 2004b; Tripathi & Pandey 2004; Tripathi & Singh 2001; Chaurasia 1995). There are other herbal combinations with similar potential for the treatment of rheumatoid arthritis (Chopra 2011). There are also recent investigations that have suggested potential benefits for osteoporosis (Tripathi 2008).
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Cashew Nut Oil: A Versatile Product All Oils are Not Equal African samples of the fresh Cashew nuts have shown a variable oil content, ranging between 15–20 per cent, while Indian samples contained 25–30 per cent (Burkill 1985). More recent Indian studies gave similar results (dos Santos & de Magalhaes 1999).
The oil of the Cashew nut (kernel) differs substantially from the dark brown-black juice of the nutshell – or the milky juice (or gum) that exudes from incisions in the tree trunk. The two forms of Cashew ‘oil’ have quite different properties (Akinhanmi 2008; Axtell & Fairman 1992): • The fine quality light yellow oil rich in oleic acid (68–80%) that is extracted from the kernel is like almond or olive oil and has similar soothing and emollient properties. Although it is not produced commercially, the oil can be useful for the preparation of liniments and ointments, and has been used as an antidote for irritant poisons in the gastrointestinal tract. • A dark viscous nut shell oil (up to 35% is found in the shell) that is particularly valuable for industrial purposes. It has unique properties that suit it for making coatings (paint, varnish, surface coatings), moulded products (including plastics), and for use as a chemical intermediary, including the production of foundry chemicals. These oils differ in their drying properties. The edible kernel oil has a non-drying character, while the cashew nut shell liquid (CNSL, cardanol) is a non-edible drying oil with numerous industrial applications9 (Akinhanmi 2008). The nut shell liquid comes in two forms: solvent-extracted immature CNSL, and technical
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CNSL that differ in their chemical composition (de Lima 2008): • Solvent extracted liquid (iCNSL): high anacardic acid levels (60–65%), with a moderate content of cardol (15–20%) and low levels of cardanol (10%). • Technical CNSL: the quality can vary according to the roasting process undertaken. It has a high cardanol content (83–84%), with a low cardol component (8–10%). CNSL has been employed in the manufacture of resins, laminating and impregnating materials, industrial belting, brake linings, for reinforcing for synthetic rubber, as a waterproofing agent, and in insulating materials. It has insulation properties that are particularly well suited for use in aeroplane ignition systems. Cardanol, a refined non-irritant form of shell oil, can be used as a fixative in perfumes or as a plasticiser for cellulose acetate lacquers (Burkill 1985; Watt & BreyerBrandwijk 1962; Quisumbing 1951). Cashew nut shell liquid (CNSL) and the kernel within the nut are commercially valuable, although unprocessed Cashew nuts have substantial poisonous potential. It is only after being detoxified that they can be utilised. This can be a complex business. Sophisticated extraction strategies are needed that will not damage the oil quality, the nut itself, and minimise toxic reactions. The application of heat (roasting in a pan, drum or ‘hot oil’ roasting) is an essential part of processing. This turns the extremely tough, leathery nut shell brittle, which is easier to crack. The nuts are pre-soaked in water, which raises the moisture content of the kernel, thereby providing protection from over-cooking. The shell also becomes more flexible and is therefore less likely to be damaged during the extraction process.
9 Oils are classified as drying, semi-drying or non-drying according to their iodine value. A low iodine value indicates a low content of unsaturated fatty acids. Because the iodine value of cashew kernel oil is lower than 100 mg/100 g it is classified as a non-drying oil. In comparison, the CNSL iodine values are high (215–235 mg/100 g) with drying properties applicable for use in paints, varnishes etc. However, neither form of oil is suitable for soap-making purposes due to low saponification values, nor are they suitable for animal feed purposes due to their low ash content, which indicates a low mineral content (Akinhanmi 2008).
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Oil collection strategies need to avoid human exposure as even the fumes have toxic potential. Fortunately, the heat chemically changes the shell oil. This alters (decarboxylates) the irritant anacardic acids into the less allergenic compound cardanol, which predominates in CNSL. The efficacy of the process depends on the technique utilised. For commercial purposes, oil collection usually requires special roasting equipment which prevents damage to the nut and maintains the quality of the nut shell oil – which can increase the cost of processing, significantly. After roasting, the nuts can be cracked manually (making sure gloves are worn) or with mechanical blade openers. After extraction, the shelled nut kernels are dried and cleaned (e.g. tumbled in sawdust or ash) to remove any excess oil. The testa is then removed (peeled off) and the kernels graded for product quality (practicalaction. org/docs/technical).
Cashew Nut Processing Pan roasting involves heating in a pan over an open fire. The shell oil ignites and burns off with a smoky black flame, cooking the nut within. Drum roasting is similar and involves feeding the nuts into a rotating drum, during which time they are cooked and the smoke removed via a chimney arrangement. However, hot oil roasting is required to collect the CNSL. The nut is immersed into oil
Nut shelling areas – note stainless steel bowls with castor oil, to protect hands from the CNSL irritant. (Courtesy: Charlie Sellers, flickr)
and cooked, whereby the nutshell oil is infused into the cooking oil for later re-collection. Solvent extraction can be utilised for the same purpose. The level of CNSL extraction can vary, ranging from 50–90 per cent. However, because some oil remains in the nuts they should be handled with care. The temperature of the process also requires careful control to prevent polymerisation of the CNSL (practicalaction.org/docs/technical; Axtell & Fairman 1992). The Cashew tree did not attract a great deal of innovative interest for a long time – a situation that has changed in recent years. A focus on natural renewable sources of fuel such as ethanol has lead to the suggestion that Cashew apple bagasse10 may be suitable for ethanol production, similar to the current use of Cashew apple juice or sugar cane juice (Araújo 2010; Rocha 2010, 2009; Paceco 2010; Chelikani 2009). New technologies have investigated the production of emulsification agents (biosurfactants) from Cashew apple juice (Giro 2009). The antibacterial properties of anacardic acid and cardanol have made them good candidates for producing anti-fouling polymers (polyanacardic acid and polycardanol coatings) for use in marine environments (Chelikani 2009). In addition, Cashew gum has been proposed as an alternative to gum arabic, which is relatively expensive, for microencapsulation purposes. This involves the preservation of materials rich in volatile compounds (e.g. coffee) by spray drying (vaporisation) to remove the water component without the loss of characteristic fragrance or flavour attributes (Rodrigues & Grosso 2008). Another interesting development is the production of an adhesive from cashew shell nut oil that reduces formaldehyde and VOC (volatile organic emissions) from engineered wood products such as flooring (Kim 2010).
10 Bagasse is the fibre left over once the juice has been extracted. Sugar cane bagasse is the source of a biofuel. Australia has large sugarcane bagasse resources – for each 10 tonnes of sugar cane crushed, 3 tonnes of bagasse are created.
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Cashew – A Useful Insecticide?
Hyaluronic Acid
Hyaluronic acid has been extracted from animal tissue, notably rooster combs. (Courtesy: Hershel K. Gattis, flickr)
Cashew apple juice is suitable for hyaluronic acid production using bacterial fermentation techniques. This polysaccharide, which is naturally present in many body tissues (the highest concentrations are found in the eye and joints) has gained popularity as an antiarthritic agent. It has been employed for rheumatoid arthritis and osteoarthritis to help maintain joint integrity, although the injection needs to be repeated every 8–9 months. At this time, however, the treatment is considered unproven as the clinical results can be variable, with some finding it effective and others gaining no relief. Doubtless further research will improve product bioavailability and lead to a more specific understanding of its practical utilisation by the body. Hyaluronic acid has a few other interesting clinical applications due to its water-retentive and wound-healing qualities. It has recently become more widely used in cosmetics and pharmaceuticals due to its high visco-elasticity and ability to retain large amounts of water. In plastic surgery it is employed to make the skin appear less sagging or wrinkled (e.g. as a lip ‘filler’). Hyaluronic acid has also been utilised in eye surgery, injected into the eye to counteract fluid loss. The microbial production of hyaluronic acid using natural mediums such as Cashew apple juice would mean a reduction in production costs, as well as the risk of microbial contamination, with the potential to significantly increase production levels. Hyaluronic acid currently costs US $2,000–60,000 per kg, depending on the quality required (Pires 2010).
Flowering Cashew tree.
The Cashew tree (Anacardium occidentale) has long been valued as an insecticidal agent. In Asia, the oil was often painted on floors and housing timbers to preventing termite attack, while bookbinders used the gum (which has adhesive properties) as well as the oil for preventing moth or ant infestations. These uses are supported by studies showing extracts possessed insecticidal activity against weevils and moth larvae. Larvicidal
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properties against mosquitoes have been demonstrated and, rather surprisingly, potential for use as an attractant in mosquito traps (Mukhopadhyay 2010; Santos 2010; de Mendonça 2005; Evans & Kaleya Raj 1988; Watt & BreyerBrandwijk 1962). The larvicidal components were identified as anacardic acid, cardol and cardanol. In addition, these components and CNSL have exhibited anti-acetylcholinesterase (AChE) activity – an enzyme-inhibitory effect utilised by many insecticides11 (Oliveira 2010). Brazilian researchers have suggested the use of sodium anacardate as a non-toxic insecticide against Aedes aegypti – the mosquito vector for dengue fever and yellow fever (Farias 2009). In addition, Anacardium occidentale extracts have shown varied anti-parasitic actions that are of interest – specifically against nematodes (worms), leishmania and filaria. This activity is probably linked to anacardic acids, and the derivatives cardol and anacardol, which were found to have good antibacterial and anthelminthic properties (Oliver-Bever 1986). In Brazil the Cashew has been used in the treatment of skin ulceration due to leishmaniasis. Studies showed extracts had various levels of activity against this parasite (anti-leishmanial properties), as well as its snail host (molluscicidal action). Anacardic acids were particularly active molluscicides. Unfortunately, field trials in Mozambique revealed that use of the extract in mosquito-breeding sites was limited because the treated water caused dermatitis (Evans 2002; Franca 1996; Jurberg 1995; Franca 1993; de Souza 1992; Mendes 1990; Schultes & Raffauf 1990; Suresh & Raj 1990; Laurens 1987; Garg & Kasera 1982).
11 This type of drug can have potent effects on the nervous system, depending on the dose and specific effects of the chemical utilised. AChE has an important role in neurotransmission via its effect on the excitatory neurotransmitter acetylcholine, which it hydrolyses into choline and acetic acid – a process that prevents over-stimulation of neurological functions. Inhibitors of AChE have not only provided pesticides, they have been utilised as chemical warfare agents, some of which have serious neurological toxicity (Oliveira 2010; De Lima 2008).
Garden Geranium (Pelargonium x hortorum). Pestresistant Geranium plants can contain high levels (up to 81%) of anacardic acids (i.e. omega-5 anacardic acids) – which are involved in the resistance of some species toward spider mites and aphids.12 Plants with a high level of resistance against insect pests can utilise these compounds better the low-resistance species of varieties (Lis-Balchin 2002; Schultez 1996; Grazzini 1991). Anacardic acid purified from the Garden Geranium (Pelargonium x hortorum) has shown an inhibitory activity on breast cancer cell lines, indicating substantial anticancer potential (Schultz 2011). (Image courtesy: Queerbubbles, Wikipedia, CC-by-SA3.0)
Anacardium: A Caustic Healing Agent
Henry Burkill (1935) observed with regard to the inflammatory properties of the Cashew resin: ‘Cardol from Anacardium is not identical with a substance from Semecarpus anacardium to which the same name has been given, but is similar and is less irritant. However, both cause an inflammation, like erysipelas, with pustules on the skin: taken internally into the intestine, they cause gastro-enteritis with loss of control of the muscles and interrupted respiration. The action on the skin has been compared in intensity to cantharidin; but in the intestine it is feebler.’ Despite its strong vesicant nature the nut oil has been utilised in diverse cultures as a healing agent. Its irritant characteristics have been employed in treatments for ringworm and as a cosmetic abrasive 12 The ornamental garden Geranium belongs to the genus Pelargonium (commonly known as Storksbills) which contains innumerable cultivated hybrids and varieties. Many are valued for their aromatic qualities. Confusingly, another rather large classification of small flowering herbs (around 420 species), known as Cranesbills, belongs to the genus Geranium. Both Pelargonium and Geranium belong to the family Geraniaceae.
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Anacardium, from Dr SR Phatak, Materia Medica of Homoeopathic Medicine (1977). The text outlines the main indications for the use of Anacardium, although the full listing extends to another two pages. Anacardium is well known as a remedy for emotional distress, stress-induced headaches, memory disorders, and mental fatigue due to excessive intellectual demands including intense research and study.
to remove unsightly blemishes or growths (e.g. warts, corns). It was even found useful for treating cancerous ulceration and leprotic sores. In Medicinal Plants of East and Southeast Asia (1980), Perry and Metzger include this caution: ‘The gum resin from the fruit wall causes dermatitis just as the sap from some species of Rhus, and use of the oily substance from the pericarp on warts, callosities, corns, and cracks in the soles of the feet, at times produced symptoms of poisoning, so this practice has been discontinued.’ The level of irritation could vary, depending on whether the mix was heated. Needless to say, the effects of the resin could be quite drastic. Those unskilled in its use could inflict substantial (often irrevocable) skin damage (Watt & Breyer-Brandwijk 1962; Burkill 1935; Grieve 1931). Various other remedies have employed the oil; it would appear that the significant antibacterial properties of anacardic acid contributed to its reputation. The juice from the Cashew apple (the pedicel), and the nut oil, have been employed as antisyphilitic and wound healing agents. In Africa, the
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sap and the oil were used for treating the ulceration associated with leprosy – particularly as an ointment formulation (Burkill 1985). In Southeast Asia the pericarp oil was applied as an anaesthetic for leprotic affections (Quisumbing 1951). In South America the oil of Caju (Anacardium humile) was likewise utilised as a leprosy remedy (FAO 1986). African healers in Ghana employed a decoction of Cashew roots (without the bark) as a healing bath for yaws on the soles of the feet (Burkill 1985). A similar preparation was used in the Philippines for the treatment of diabetes and syphilitic joint swelling (Quisumbing 1951). Experimentally, leaf and cashew nut shell extracts have shown cytotoxic activity and anticancer potential that are linked to their anacardic acid and cardol components.13 Recent research has investigated the use of anacardic acids as a basis for anticancer and antibacterial drug design – including activity against the drug-resistant (MRSA) Mycobacterium smegmatis, and the cariogenic Streptococcus mutans (Kubo 2011; Konan 2010; Logrado 2010; Schultz 2010; Chandregowda 2009; De Lima 2008; Kishore 2008; Sung 2008; Green 2008, 2007; Barcelos 2007a, 2207b; Swamy 2007; Singh 2004; George & Kuttan 1997, Banerjee & Rao 1992). In addition, flavones from the Anacardiaceae have attracted some interest. Agasthisflavone, isolated from Cashew leaf extracts, has shown anti-leukaemic potential (Konan 2010). This compound (which is also present in species of Rhus), and a number of related flavones, have been of interest for their antiviral activity (e.g. against hepatitis B, Herpes simplex and HIV) and potential effects on nervous system function (Lin 1999, 1997; Svenningsen 2006; Nakano 1998; Svenningsen 1998; Wang 1998). Anacardic acid has also been investigated as a substitute for salicylic acid (aspirin) in the development of sildenafil analogues – a class of drug that has been utilised for the treatment of erectile dysfunction. Unfortunately, anacardic acid is associated with side-effects that limit its usefulness, and thus investigations continue to evaluate alternative resources with similar activity – that is, phosphodiesterase-5 (PDE5) inhibitory properties (Paramashivappa 2002). 13 Urushiols isolated from the sap of the Korean lacquer tree (Rhus vernicifera) have likewise shown cytotoxic activity (Hong 1999).
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New Uses for an Old Gum
that gives it adhesive qualities. The gum, which is largely insoluble in cold water, is somewhat more soluble in hot water, which makes it suitable for use as a form of ‘Gum arabic’.14 This demulcent pharmaceutical additive has innumerable practical uses in pharmacy – for example, in cough mixtures and throat lozenges, and in antidiarrhoeal preparations. While the usefulness of Cashew gum has, in the past, been limited due to potential contamination with the irritant sap, modern purification strategies have resolved the problem, enabling its use in a great range of products (da Silva 2002): • pharmaceutical and cosmetic preparations: as a gelling agent in capsules and pills; • food industry: as a stabilising compound in juices, beer and ice cream, and as a clarification agent in juices; • liquid glue alternative for stationery; • potential for making inks and varnish; • wine-making purposes; biochemical applications, e.g. the use of • thepurified polysaccharide for making the hydrogels used in lectin studies.
Cashew tree.
Cashew or Acajou gum (the bark exudate) is a complex polysaccharide-based product (high levels of galactose, with smaller amounts of arabinose, rhamnose, glucose, mannose and galacturonic acid) with associated mineral ions (potassium, sodium, calcium, magnesium) (da Silva 2002). It has a mucilaginous character
Cashew ‘Apples’ Cashew fruit with orange pedicel. (Courtesy: Marcelo de Souza Pereira, flickr)
14 This product was originally sourced primarily from Acacia senegal, although a few other species of Acacia are suitable. Gums, which have colloidal properties, can be used to produce gels with high-water absorptive characteristics. This effect is used by young plants as a protective strategy against stress due to water loss (de Silva 2002).
The Cashew pedicel (Cashew ‘apple’) has an intriguing mode of development. The nut forms first a case-like shell with a honeycomb-like outer covering in which the nut shell liquid develops. The seed within is separated by a thin casing. When the nut is fully formed, albeit still unripe, the base (the peduncle or receptacle) begins to grow. This develops into a juicy plump fruit, with a somewhat spongy and fibrous character. Although edible when ripe, the yellow-red skin has a distinct waxy texture and, when eaten, the fibrous residue is discarded. The juice has a mild acid flavour. (Continued p. 221)
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Table 6.2 Medicinal uses of the Cashew tree (Anacardium occidentale) and supportive investigations
Over time the Cashew Tree achieved an interesting medicinal reputation. The tree has not only been popular as an anti-diarrhoeal remedy, it also has a good reputation as an anti-diabetic, analgesic, anti-inflammatory and antibacterial agent. Category of use
Traditional uses (reference)
Investigations
Antidiabetic
The bark was known as ‘diabetes bark’ in the Philippines, while Malaysian remedies used the water in which the bark was boiled as a sugar-lowering agent. These effects have been verified experimentally.
Extracts of the stem bark and leaf have shown a protective action against experimentally induced diabetes in animals – with some investigations showing a kidney protective effect (Sokeng 2007; Tedong 2006; Olatunji 2004; Ojewole 2003).
In Ayurvedic medicine the fruits and leaves Studies have suggested that compounds in the herb can were likewise employed as a hypoglycaemic affect insulin metabolism and thereby influence obesity. remedy (Zakaria & Mohd 1994; Kamtchouing In addition, enzyme inhibitors in Cashew shell nut 1998; Swanston-Flatt 1989; Burkill 1985; liquid have shown a significant effect on carbohydrate Quisumbing 1951). metabolism and have potential for influencing digestive enzyme function (Toyomizu 1993). Cardiovascular
India: tincture or bark extract lowers blood Leaf and bark extracts: hypotensive activity. pressure (Chopra 1956). Anti-hypertensive effect possibly due to vasodilation of the peripheral blood vessels (Garg 1992; Oliver-Bever 1986). Studies of Cashew leaf extracts suggest vasodilatory potential that may be useful for cardiovascular disorders (Runnie 2004).
Anti-ulcer
Leaf and bark infusions utilised as a remedy Extracts of Anacardium occidentale and A. humile have for gastric ulceration and gastritis. shown gastroprotective and antiulcerogenic activity (Konan & Bacci 2007). Anacardic acid appears to be active as an antioxidant and gastroprotective agent (Morais 2010; Luiz-Ferrera 2010; Jaiswal 2010).
Antimicrobial
Numerous medicinal uses in North and South America: infusions or maceration of bark and/or leaves employed for skin disorders (eczema, psoriasis), syphilis-related skin problems, venereal disease and urinary disorders, respiratory problems (asthma, cough, bronchitis), ENT (tonsillitis, mouth ulcers, throat problems) (Taylor 1998).
Investigations have shown a broad spectrum of antimicrobial activities for many parts of the Cashew Tree (Oliver-Bever 1986). Studies have shown stem bark and leaf extracts had activity against Staphylococcus aureus, Streptococcus spp. (S. faecalis, S. pneumoniae, S. albus), and Klebsiella pneumoniae – with methanol extracts being the most efficacious (Abulude 2009).
Nigeria: Cashew is incorporated into numerous herbal recipes for the treatment of An Indian study has confirmed that leaf ethanol extracts asthma (Sonibare & Gbile 2008). were effective against Staphylococcus aureus and Bacillus subtilis, as well as possessing antifungal activity against Africa: Nigerian healers utilised an infusion of Candida albicans and Aspergillus niger (Dahake 2009). the leaves and bark as a mouthwash to ease toothache and sore gums. Nigerian tests of Cashew extracts confirmed antibacterial properties against gram-negative bacteria (Escherichia Asia: Java (Indonesia) a paste of the old leaves coli, Pseudomonas aeruginosa). The bark extract was applied to skin disorders, including a also had activity against a drug-resistant form of condition known as pemphigus neonatorum Klebsiella pneumoniae (against which streptomycin was (dermatitis of the newborn) (Oliver-Bever ineffective). This was of particular interest (Akinpelu 1986; Burkill 1935). 2001; Kudi 1999; Mackeen 1997). Indonesia: older leaves with other remedies Leaf essential oil has shown similar antibacterial potential poulticed on burns and skin diseases. Very (Garg & Kasera 1984). effective (Perry & Metzger 1980). The antimicrobial properties of the nut shell oil are Pedicel juice very astringent: used as potent, an activity attributed to anacardic acid (Kanojia mouthwash and gargle to treat quinsy – 1999; Himejima & Kubo 1993). Investigations of peritonsillar abscess (Perry & Metzger 1980). anacardic acid and totarol* against drug-resistant forms of Staphylococcus aureus showed anacardic acid to be
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Indonesia: older leaves with other remedies poulticed on burns and skin diseases. Very effective (Perry & Metzger 1980). Pedicel juice very astringent: used as mouthwash and gargle to treat quinsy – peritonsillar abscess (Perry & Metzger 1980).
Leaf essential oil has shown similar antibacterial potential (Garg & Kasera 1984). The antimicrobial properties of the nut shell oil are potent, an activity attributed to anacardic acid (Kanojia 1999; Himejima & Kubo 1993). Investigations of anacardic acid and totarol* against drug-resistant forms of Staphylococcus aureus showed anacardic acid to be the more effective, although their activities were also synergistic (Muroi & Kubo 1996; Kubo 1992).
Antibacterial properties of the ‘vapour form of the oil’ were compared to that of Chaulmugra oil (from Hydnocarpus wightiana), which has been utilised for treating leprosy, although it was ‘considerably inferior to Chaulmugra’ (Burkill 1935).
Stem extracts have shown activity against oral (dental) bacteria. Anacardic acid was particularly effective against Streptococcus mutans (which is responsible for tooth decay) and the acne-causing bacteria Propionibacterium acnes. Anacardium humile has similar potential (Pereira 2010; Green 2008; Kubo 1993).
Anti-influenzal potential: juice of the fleshy peduncle used to treat influenza in the Amazon (Schultz & Raffauf 1990).
Antibacterial activity against Helicobacter pylori was exhibited by anacardic acid and hexenal isolated from the Cashew apple (Kubo 1999). Derivatives of cardanol (decarboxylated anacardic acid = CNSL) have antifungal activity (Bolton 1994). Cashew tree leaf extracts have antifungal activity against Cryptococcus neoformans (Schmourlo 2005). Cashew nut shell liquid has also been evaluated as an antibacterial feed additive for farmed animals (ruminants) with potential to reduce the intestinal fermentation that leads to gaseous methane emissions (Watanabe 2010).
Analgesic and antiinflammatory
Skin of seed applied to forehead and temples as headache cure (Perry & Metzger 1981).
Leaf essential oil: central nervous system depression of tranquilliser type, with an added analgesic effect (OliverBever 1986).
Massage oil for rheumatism: extracted by boiling liquid extract of triturated pericarps with seeds and water (Perry & Metzger 1980).
Antidiarrhoeal
Oil of pericarp useful as an anaesthetic in leprosy and psoriasis; used as a blister for warts, corns and ulcers (Quisumbing 1951). In South America, Africa and Asia the Cashew tree (bark, leaves, sometimes tree sap) was often utilised for making astringent remedies. Young leaves widely used for treating dysentery, diarrhoea and haemorrhoids. South America: fruit juice, bark, leaf and fruit wine used as antidiarrhoeal and antidysenteric remedies (Taylor 1998). Philippines: receptacle boiled in sweetened water as a remedy for dysentery (Perry & Metzger 1980). Similar uses were reported from Africa, India, Southeast Asia and the Pacific Islands (Oliver-Bever 1986; Mota 1985; Burkill 1985; Burkill 1935).
A substantial amount of tannin (up to 23%) can be present in the leaves and the bark of Anacardium occidentale. The antiinflammatory and antibacterial properties of tannins would certainly have contributed to its efficacy and would support many other traditional uses of the plant (Taylor 1998). There is a report that suggests Anacardium occidentale leaf infusions can regulate colonic fluid metabolism by promoting water and sodium resorption and thereby reduce the potential disastrous effects of dehydration (Yusuf 2009).
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Genitourinary disorders and fertility
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Contraceptive agent: the bark decoction has been taken during the menses for this purpose in the Amazon. Anacardium microsepalum has been utilised similarly (Schultes & Raffauf 1990). Stomach pain: In the Congo a decoction of Cashew tree bark and Manilkara obovata has been taken to ease stomach pains in women (Burkill 1985). Urinary disorders: bark has been used as a remedy for urethral discharge (Burkill 1985). Abortion: Indian folk remedies employed the irritant effects of the crushed Cashew nut to induce abortion (Burkill 1935).
* Totarol, which has substantial antimicrobial potential, is present in many species of Podocarpus, a genus of trees that is native to the Australian rainforest.
Cashew ‘Apples’ (continued) Cashew apple is a very versatile fruit. It has been used as a candied sweet and a dried fruit, as well as for making preserves, vinegar, non-alcoholic drinks and wine. Indeed, the fruit juice has been made into alcoholic beverages around the globe – Africa, the West Indies, South and Central America. A Cashew apple wine has been popular in Mozambique and Ghana. In Goa, India, a local liquor known as feni was quite famous (Morton 1986). The distilled spirit has even been reported to be ‘better than arrack or rum’ (Grieve 1931). The bark of the Brazilian Caju, Anacardium humile, has been macerated in sugar cane spirits to make a liqueur that was also reputed to be an aphrodisiac (FAO 1986). The Cashew fruit has a wide range of medicinal uses. Fresh or distilled, the juice was reputed to have potent diuretic properties, as well as a sudorific action (inducing perspiration). Brandied, the juice even provided a liniment for easing rheumatic and neuralgic pain (Morton 1986). In Asia, an oil-based massage liniment was used as an anti-rheumatic rub. The juice has been taken to quell nausea and vomiting, to ease a sore throat, as well as being utilised as a mouth wash for thrush or as a gargle for catarrh. In the Philippines a sweetened tea made from the pedicel was taken for dysentery, while the seed skin could be applied to the forehead and temples for hea da ch e
The Cashew apple has a good carbohydrate rating (9.8%) similar to apples, mangoes and red grapes. Studies have shown that the juice contains good levels of vitamin C (77 mg%) and polyphenols (1.7 mg %CE, catechin equivalent). However the carotenoid component is lowmoderate (0.28 mg%). In comparison, the carotenoid level in Papaya, Surinam cherry, Mango and Acerola is higher (1.61–1.87 mg%). The Surinam cherry is also high in polyphenols (1.77 mg% CE), with Passionfruit rating even higher (2.28mg% CE). Vitamin C levels in the Acerola are extremely good (224.57 mg%) – with the lower levels being found in the Surinam cherry, kiwifruit, lemon, pineapple and Papaya (45–58 mg%) (Spada 2008). (Image courtesy: Abhishek Oommen Jacob)
relief (Perry & Metzger 1980; Burkill 1935). In Senegal the fruit syrup, which was valued as a general panacea, was recommended as a stimulant, general strengthening tonic, ‘elixir of longevity’, and even had a reputation as an aphrodisiac (Burkill 1985).
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Nutritional Nuts
The Cashew nut has a good nutritional value due to its content of protein (amino acids), fats (lipids) and vitamins. The main mineral components (mg/100 g) of the Cashew nut are potassium (27.5 mg), calcium (21.5 mg), magnesium (19.3 mg), sodium (8.2 mg), phosphorus (14 mg), zinc (0.8 mg) and iron (0.6 mg) (Akinhanmi 2008). The protein level (mg/100 g) is fairly good (18.81 mg) when compared to other nuts. The level in almond, pistachio and Virginia peanut (19–21 mg) was slightly higher. The level in Brazil nut, pine nut and walnuts was slightly lower (13–14 mg), while that of pecan and macadamia nuts was substantially lower (7–8 mg) (Venkatachalam & Sathe 2006). However, processing methods can substantially alter these nutritional components. Raw cashew kernels contain appreciable amounts (mg/100 g) of carotenoids (β-carotene 9.57 mcg, lutein 30.29 mcg, zeaxanthin 0.56 mcg), vitamin E (α-tocopherol 0.29 mg, y-tocopherol 1.1 mg), thiamine (1.08 mg) and fatty acids (stearic acid 4.96 g, oleic acid 21.87 g, linoleic acid 5.55 g). An analysis of conventional shelling methods that involve roasting (oil-bath, steam and open-pan roasting) and drying revealed a significant reduction in these compounds. However, a traditional hand-cracking technique (the Flores method, which uses a simple hand-operated machine) retained the nutritional integrity of the nut (Trox 2010). Maintaining the nutritional integrity of the nut is important for the associated health benefits. The incorporation of a variety of tree nuts into the diet has been linked to a lower risk of obesity and weight gain, enhanced antioxidant status, cholesterol-lowering effects, a reduced risk of cardiovascular disease and benefits for diabetic individuals (Trox 2010). One study has shown a significant reduction in the risk of coronary heart disease (35% risk reduction) in women who ate nuts five times per week – as compared to those who ate them infrequently (Hu 1998). Many nuts have cholesterol-lowering effects (walnuts, macadamia, pecans, pistachio, almonds, peanuts). Although nuts are generally rich in fat (lipids), they contain the right type of fat (i.e. monounsaturated and polyunsaturated) with a good fatty acid profile. Therefore, while the total oil content can be quite
high – for example, Brazil nut 61%, pecan 58%, pine nut 59%, pistachio 51% and cashew 40%15 – there is a high proportion of unsaturated fatty acids. For instance, cashew contains oleic (57%) and linoleic (21%) acids, with substantially lower levels of the saturated fatty acids (palmitic acid 10% and stearic acid 9%). Cashew oil also contains a fair amount of vitamin E (α- and y-tocopherol: 61 mg/g) and squalene16 (89 mg/g). However, the level of vitamin E in some other nuts can be quite high (mg/g oil): Brazil nut (199 mg), pecan (181 mg), pine nut (229 mg), pistachio (291 mg). Squalene levels in Brazil nuts can be very high (1377 mg), with lower levels in pecans (152 mg), pistachio (91 mg) and pine nuts (40 mg). Vitamin E and squalene are of interest as they have potent antioxidant potential with supportive effects on cardiovascular health; squalene is also an important steroid precursor that has attracted particular interest as an anticancer agent (Ryan 2006). Sterols may also contribute to the cholesterol lowering effect of nuts, which tend to have quite high levels of β-sitosterol in the oil (cashew 1768 mg/g, plus campesterol 105 mg/g, and stigmasterol 117 mg/g) (Ryan 2006). In comparison, β-sitosterol and stigmasterol levels in the oil component of pistachio are high (4686 mg and 663 mg respectively), with the levels in other nuts generally being somewhat lower: Brazil nut (1325 mg and 577 mg), pecan (1572 mg and 340 mg) and pine nut (1842 mg and 680 mg). Campesterol levels ranged from being comparatively low in the nut oil from Brazil nuts (27 mg) and pecans (52 mg), to higher levels in pine nut (215 mg) and pistachio oil (236 mg) (Ryan 2006). Investigations of Cashew extracts (tree stem bark, cashew nut shell) have shown antioxidant, anti-mutagenic and anti-genotoxic activity.17 The antioxidant activity of many Cashew products can be linked to their phenolic component – anacardic acids, cardol and cardanol (Oliveira 2010; Trevisan 2006). 15 There can be considerable variation in lipid levels in some studies. Another review provided the following analysis of lipid levels in Brazil nuts, macadamias, pecans, pine nuts and walnuts : 61–66 g/100 g; almonds, cashews, pistachio and Virginia peanuts: 42–45 g/100g. Certainly cultivar and growing conditions will have a significant influence. For greater detail see Venkatachalam & Sathe 2006. Amino acid profiles are also reviewed in detail in this paper. 16 Olive oil is a particularly rich source of squalene (2,000–7,000 mg/g oil). 17 Cashew apple fresh and processed juices have also demonstrated antimutagenic properties (Melo-Cavalcante 2008, 2003).
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The level of total phenolics in the leaf extract has been evaluated at 35.5 per cent18 and the flavonoid content at 2.58 per cent (Konan & Bacci 2007). Processing can substantially alter the level of these components. For example, Cashew nut shell liquid contains a higher level of phenolics (anacardic acids 353.6 g/kg) in comparison to the roasted nut (0.65 g/kg). The Cashew apple and fibre contain anacardic acid, while cardanols and cardols were more abundant in the nut shell liquid. However, the Cashew nut (raw and roasted) itself contains low amounts of phenols (Trevisan 2006). Despite thse valuable attributes, serious concerns with regard to nut allergies extend to the Cashew. While the most often cited culprit is the peanut (a ground nut), Cashew tree nuts can be equally problematic, if not more so, and there is an associated risk of anaphylaxis that should not be underestimated (Davoren & Peake 2005).
Nut Phenolics
Overall, many nuts contain polyphenolic components (proanthocyanidins, flavonoids, resveratrol) of dietary interest - although the total phenolic content of the different tree nuts can vary substantially (103–1650 GAE/100 g) (Bolling 2010). Pecans, walnuts and pistachios show the highest values – which compare very favourably with blueberries (531 mg), plums (367 mg) and raisins (1065 mg). The level of resveratrol,a stilbene with anticancer potential, can range quite dramatically – e.g. peanuts (3–192 mcg/100 g) and pistachio (9–167 mcg/100 g) – in comparison to the fairly high level found in red wine (98–1800 mcg/100 ml) (Bolling 2010). Mixed nuts. (Courtesy: Melchoir, Wikipedia)
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The Mango Tree
The Mango tree (Mangifera indica) is a common urban tree of northern Australia that has become widespread in the wild. Even though it can be considered an intrusive weedy nuisance in some places, many native animals have come to rely on its seasonal flowering and fruit crop. The yellowish sap found throughout the trees’ tissues (trunk, branches, leaves) oozes readily from the wounded skin of unripe fruits or the cut fruit base. It becomes translucent upon drying and has good adhesive qualities. It has even been used to mend broken crockery. However, Mango sap has irritant qualities that are common to the Anarcadiaceae. Even contact with Mango leaves or, for some people, the fruit, can have serious allergenic effects – dermatitis (skin reddening, possibly blistering), itching and puffiness of the eyes, as well as respiratory difficulties. Excessive ingestion of the fruit has even been associated with renal inflammation.19 Mango leaves contain a glucoside (mangiferine) that is poisonous to animals and cannot be used as fodder unless detoxified. In India, the use of the leaf as cattle feed induced the production of ‘peori dye’ or Indian yellow, a rich yellow dye (euxanthic acid) that was extracted from the animals’ urine. This was a cruel practice with a high incidence of animal fatalities due to renal failure and was eventually outlawed (Morton 1986). A couple of other species have similar toxic potential. The caustic juice of Mangifera foetida has been used to deepen tattoo scars – while the deliberate application of the unripe fruit skin can also produce inflammation. However, a lotion made from the bark was utilised for treating ulceration, and in Indonesia the roasted seed kernel provided a remedy for itching skin problems. The sap of Mangifera caesia has even been used criminally to cause injury by inflicting skin damage, or ingested to incite vomiting and purging (Burkill 1931; Perry & Metzger 1980).
18 Jaiswal (2010) also provides total phenolic values for leaf extracts as a gallic acid equivalent (GAE): methanolic extract 40–26 (GAE/mg extract); aqueous extract 37.41 (GAE/mg extract). 19 Reaction to the sap from the Marking Nut tree (Semecarpus anacardium) has also been implicated in renal damage (Matthai & Date 1979).
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The Genus Mangifera The Mango is among the most famous of the Asian tropical fruits. Native to eastern India, Burma and the Andaman Islands, it has been in cultivation across Asia since antiquity. Around the fourth or fifth century BC, Buddhist monks were reputed to have facilitated its spread on their travels to Malaya and eastern Asia. The Persians carried it to East Africa around 1000 AD. It appears that they chose wisely. Mangifera indica is, indeed, the best candidate for cultivation from the genus. Although there are around 40 species, only a few have been utilised for their fruit or in making pickles. These include Mangifera sylvatica
mangiferol and mangiferone. The dried flowers, which also contain tannin (15%), have been used as an astringent for the treatment of diarrhoea, chronic dysentery and genitourinary disorders (bladder catarrh, chronic gonorrhoeal urethritis) (Morton 1986, 1982; Quisumbing 1951).
Blooming Mango tree and flowers
Mango tree.
of the eastern Himalayas, Nepal and the Andaman Islands; the Asian Horse Mango (M. foetida), and M. caesia of Malaysia and the Philippines. Mangifera longipetiolata, M. maingayi and M. kemanga can be found in cultivation around Malayan villages. Only a few species appear to have a medicinal reputation, which is limited by their irritant potential. Sensitive individuals can suffer serious discomfort (facial swelling and burning, rash, dyspnoea) when the Mango tree is in bloom – even though there is no airborne pollen. The few pollen grains that the tree produces are large and tend to adhere to each other, even in dry weather, and thus are not dispersed in the atmosphere. The irritant agent appears to be found in the vaporised essential oil of the flowers, which contains
An Extensive Medicinal Reputation The Mango tree has a comprehensive medicinal reputation (Ross 1999; Morton 1986; Burkill 1985; Quisumbing 1951): • African traditions recommended bark and leaf decoctions for gastrointestinal problems (diarrhoea, dysentery) and the bark as a diuretic for urethral discharge, as well as for treating leucorrhoea. • The bark sap was utilised in Gabon as an antisyphilitic, as was the irritant oil extracted from it. • In Zaire the stem bark was recommended for
CAUSTICS AND CORROSIVES
•
• • • •
treating chest pains, coughing, anaemia, urinary tract infections, and diabetes. In Ghana, an enema prepared from the young callus bark (from the trunk) was utilised for haemorrhoids, or employed rectally as a stimulant in wasting diseases. On the Ivory Coast, the bark decoction provided a wash for the head to treat migraine. Bark decoctions also provided a popular form of mouthwash for toothaches, sore gums and sore throat in Nigeria and the Congo. In Cambodia, hot lotions prepared from the bark were applied for rheumatic pain, and occasionally the gum solution was taken for dysentery. In the Caribbean, leaf decoctions were used in treatments that ranged from diarrhoea and fevers, to chest complaints and diabetes. The leaves have also been incorporated into tonic remedies taken after childbirth.
Most parts of the Mango tree have a reasonable tannin content: levels in the bark vary from 13–20 per cent tannic acid, with lesser amounts (8–9%) being found in the fruit and seed (Watt & Breyer-Brandwijk 1962). Mango leaves contain anthocyanidins, leucoanthocyanins, catechic and gallic acids, as well as other important phenolics (mangiferin20, isomangiferin) and flavonoids (kaempferol, quercetin). In India the astringent bark was employed to treat bleeding problems (haemorrhagic diarrhoea, haemoptysis, lung haemorrhage) and as an antidiarrhoeal agent. Its antibacterial and antispasmodic properties would contribute to its efficacy. In Gabon, the leaf decoction was recommended for treating asthma and bronchitis. Seed decoctions were used similarly for asthma in Nepal, and leaf extracts for coughs and asthma in India (Ross 1999; Perry & Metzger 1980). Various preparations have febrifugal attributes. The bark decoction (with other ingredients) was traditionally taken as a remedy for malaria in 20 Mangiferin can be present in high concentrations in young leaves (172 g/kg), bark (107 g/kg), and old leaves (94 g/kg) (Barreto 2008). However, the level can vary. Cuban studies of the Mango-based extract Vimang isolated mangiferin (71.4 mg/kg), as the major phenolic component, with lesser amounts of catechin (13.03 mg), epicatechin (8.07 mg), methyl- and propyl-gallate (4.45 mg and 4.76 mg respectively), propyl benzoate (3.99 mg), 3,4-dihydroxy-benzoic acid (2.26 mg), gallic acid (2.08 mg) and benzoic acid (1.99 mg) (Nunez-Salles 2002).
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Indonesia – although studies have not shown antiplasmodial activity. In Zaire the root decoction was utilised similarly, and in the Philippines the leaf liquid provided a bath for fevers and cold. In Nigeria the tree was popular for treating febrile illness, while in China the steeped leaves were recommended as a cooling remedy. Stem-bark extracts have shown antiamoebic activity against Entamoeba histolytica, which appears linked to their polyphenol content (Ajaiyeoba 2003; Agbonon 2002; Tona 2000, 1998; Ross 1999; Elliott & Brimacombe 1987; Perry & Metzger 1980). Mango extracts have also demonstrated anti-parasitic activity against giardia (Giardia intestinalis) (Ponce-Macotela 1994).
The Famous Mango Fruit
Mango fruits.
Mangoes on sale at a market
High-quality sweet and fragrant Mangoes are a product of selective cultivation; wild trees tend to yield fibrous turpentine-flavoured fruit that are not particularly palatable. Anti-scorbutic, invigorating and refreshing attributes that can have a useful restorative effect in heat-stroke have long been attributed to the Mango. The
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fruit contains good quantities of vitamins C and A, and the juice has been recommended as a restorative tonic. The young leaves, which have been utilised as a vegetable in Indonesia and the Philippines, also contain vitamin C. Mangoes can be extremely useful for the prevention of vitamin A deficiency, especially for children in poorer countries. This condition can have serious consequences – eye disorders (nyctalopia, hemeralopia, xerophthalmia, blindness), bone growth problems, poor immunity, growth retardation, compromised gut integrity, as well as taste and smell dysfunction, skin and sinus problems. Ripe Mangoes have been recommended as a mild laxative and diuretic. Mangoes have also had a few unusual medical recommendations associated with them. They have been noted to possess anti-haemorrhagic properties useful in the treatment of uterine, lung or intestinal bleeding. Mango juice was reputed to stop epistaxis (bleeding) if sniffed nasally. In Fiji, nasal drops prepared from the fresh kernel were utilised for sinus disorders. In Palau, the sliced and dried immature fruit was regarded as being efficacious for the treatment of septicaemia. Unripe fruit has also been used as a remedy for ophthalmia and for skin eruptions, while the astringent fruit rind, which has stimulant and tonic properties, has been recommended for debilitated individuals (Drammeh 2002; Satyavati 1987; Morton 1986; Burkill 1985; Perry & Metzger 1980). Mango peel (raw and ripe), which is currently regarded as a waste product, contains a diverse range of polyphenolic components that could have useful pharmaceutical applications. The major phenolics are protocatechuic acid, gentisic acid and gallic acid – with β-carotene being the main carotenoid (lutein and violaxanthin were also present).21 Additional phenolics of interest included mangiferin, ellagic acid, gallic acid, syringic acid, gentisyl-protocatechuic acid and quercetin (Ajila 2010).
21 Carotenoid levels in the Mango can vary quite substantially i.e.0.9-9.2gm/kg (Pott 2003).
The styptic and anti-haemorrhagic effects of the astringent Mango tree bark have long been useful for gynaecological disorders such as excessive menstrual bleeding (menorrhagia) and uterine haemorrhage (metrorrhagia), and for leucorrhoeal discharge. In Malaysia the seed extract was taken to ease menorrhagia, while in Nepal the fruit extract was used intra-vaginally for uterine haemorrhage. In India a decoction of the stem bark, sourced from a young plant (specifically one that had not yet flowered), was used for making a contraceptive: 50 g of fine stembark powder was given with an alcoholic wine. It was also said to be a safe and effective abortifacient that could be employed up to six months into pregnancy. The decoction was also taken with cow’s milk to treat menarche (the first menstrual period). Experimentally, leaf extracts have shown oestrogenic activity and an inhibitory effect on oxytocininduced uterine contractions (Ross 1999; Satyavati 1987). Among the Tikunas in the Amazon, the leaf decoction was reputed to act as a contraceptive, a cupful being taken on two successive days during the menses each month; to obtain an abortifacient effect it was taken for three days (Schultes & Raffauf 1990).
A Wound Healing Remedy
The Mango is a remarkably useful tree that has been used for all manner of healing purposes. The astringent resinous gum (76% resin, 15% gum), in combination with the emollient effects of coconut oil, has been applied to cracks in the feet, syphilitic sores, and diverse parasitic skin diseases including scabies. In Fiji the fresh leaf juice mixed in coconut oil was regarded as being useful for heat rashes and burns. In the Philippines the bark juice from the Wild Mango (Mangifera altissima) was also recommended for burns. In Zaire, Mango stem-bark (dried and infused) provided a wash for infected wounds and skin diseases, while a Sri Lankan astringent and antiseptic remedy combined Mango bark with Ervatamia dichotoma (bark, leaves) and Ficus glomerata (bark). The mix was boiled in coconut oil and applied to ulcers and fistulas (abnormal passages that often form a link between an internal abscess to other organs or to the skin) (Ross 1999; Morton 1982, 1986; Satyavati 1987; Perry & Metzger 1980; Quisumbing 1951). In Papua New Guinea, scraped Mango bark, mixed with sugar cane juice, was similarly utilised for ulcers. In Morobe province a bark infusion of the Wild Mango (Mangifera minor) was taken (or the bark chewed) for treating snakebite – while in the Sepik this remedy was utilised for centipede bites (Woodley 1990).
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Mangiferin: A Potent Mango Phenolic
Hypericum perforatum. Mangiferin has been detected in some valued medicinal herbs that originate from different botanical classifications. They include the genera Hypericum (St John’s Wort, H. perforatum and other species), Swertia (Chiretta, S. chirata, S. macrosperma, S. punctata) and Salacia (S. reticulata, S. oblonga, S. chinensis).
Mangiferin (a xanthone) has attracted interest due to its wide range of pharmacological activity– anthelmintic, antioxidant, anti-inflammatory, gastroprotective, hepatoprotective, anti-cancer, cardiostimulant22 and cardioprotective actions. Mangiferin has also shown a remarkable central nervous system stimulant properties (monoamine oxidase MAO inhibitory effect). Its benefits appear to extend to disorders such as diabetes, atherosclerosis, hypercholesterolaemia, coronary heart disease, and to liver and kidney function, as well as the immune system. It has also shown supportive effects on blood vessel formation that suggests its use in a wide range of conditions. Mangiferin has potential value for the treatment of diverse inflammatory and neurodegenerative disorders, including memory loss and Parkinson’s disease. The antioxidant properties of Mango stem-bark extracts have rated substantial 22 Indicine, which is equally widespread in the Mango tree, also has cardiostimulant actions (Kapoor 1993).
Cyclopia subternata. (Courtesy: Anne Lisa Vlok)
interest due to neuroprotective activities that prevent damage to brain cells. It can also potentiate sub-analgesic doses of morphine in rats, suggesting a role as an analgesic agent.23 The African Honey-bush (Cyclopia subternata and C. genistoides) has recently been investigated for its antioxidant and memory protective effects. The activity of the herb has been linked to mangiferin and isomangiferin. In addition, flavones (eriocitrin, nerirutin, hesperidin etc.) are present (Darvesh 2010; Joubert 2009). The herb has shown significant antioxidant, immune modulating, chemopreventive and antimutagenic activities that suggest the leaf tea would have strong protective effects against cellular damage and, possibly, environmental carcinogens (McKay 2007). Honeybush tea (the infused herb) has been recommended as a tonic for catarrhal conditions, colds and influenza – as well as for tuberculosis of the lung. It has also gained recent popularity as a treatment for menopausal symptoms (Kamara 2004).
A Versatile Antimicrobial Agent
Numerous studies of Mango tree extracts (unripe fruit, bark, stem, leaves) have shown antimicrobial activity, which is probably due to the antibacterial 23 Darvesh 2010; Daud 2010; Pardo Andreu 2010; Campos-Esparza 2009; de Paula 2009; Lemus-Molina 2009; Prabhu 2009, 2006a, 2006b, 2006c; Severi 2009; Bhatia 2008; Pardo-Andreu 2008b; Amazzal 2007; Carvalho 2007; Hernandez 2007; Gottleib 2006; Andreu 2005a; Pinto 2005; Leiro 2004, 2003; Muruganandan 2005a, 2002; Garcia 2003a, 2003b; Evans 2002; Martinez Sanchez 2001; Satyavati 1987.
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effects of mangiferin. Seed extracts have effective antistaphylococcal activity. The antibacterial action of the leaf is particularly notable against plaque bacteria. Indeed, the anti-inflammatory and antioxidant properties of mangiferin support its use in the prevention of periodontal disease (Carvalho 2009; Bairy 2002). This can help explain the deployment of Mango leaves as a dentifrice for oral hygiene, as a mouthwash for toothache, or as a gargle for sore throats. The ashed leaves, which have been a popular remedy for burns and scalds, have a styptic effect. The remedy has also been utilised as a plaster to remove warts. In Nigeria, the leaf was crushed for application to all manner of skin diseases, and studies have confirmed its activity against Sarcina lutea and Staphylococcus aureus – although it was not active against gram-negative organisms or fungi (Kapoor 1993; Satyavati 1987; Burkill 1985). Recent studies have investigated the development of mangiferin derivatives with enhanced antimicrobial applications (Singh 2009). Mango products have been used for treating eye inflammation (fresh leaf juice) and stye (petiole juice). The fact that mangiferin, which has strong antioxidant attributes, has the ability to pass through the blood–retina barrier tends to support such traditional uses of the herb and suggests potential antioxidant benefits for treating eye disorders (Hou 2010; Zhang 2010). Although antifungal studies have not shown any major activity, and studies of anti-candidal potential showed no result, the fruit peel does contain an active antifungal compound (a resorcinol derivative). Experimentally, mangiferin has demonstrated anti-herpes virus and immunostimulant properties – although prior investigations did not demonstrate antiviral attributes for leaf extracts. The related compound isomangiferin (isolated from the fern Pyrrosia sheaereri) has shown an anti-herpes effect greater than that of mangiferin. Mangiferin has also demonstrated anti-tumour and cytotoxic activity against a range of cancer cell lines (Sarkar 2004; Yoshimi 2001, Nakare 2001; Yoosook 2000; Ross 1999; Pisha & Pezzuto 1994, Guha 1996 & 1993; Zhu 1993, Zheng & Lu 1989 & 1990; Chattopadhyay 1987; Cojocaru 1986).
Mangiferin Resources
The extremely attractive red flowers of the Silk Cotton tree (Bombax ceiba) are edible. Chinese pharmacies stock the dried flower as a remedy for boils, sores and itching skin problems. The flowers and bark paste have a similar reputation in India (Kapoor 1990; Burkill 1935).
The leaves of the Silk Cotton tree (Bombax ceiba), which contain high levels of mangiferin, have shown strong antioxidant and analgesic activity (Dar 2005). This tree is native to Australia, ranging to Sri Lanka, the Himalayas and the drier parts of Malaysia. Its common name originates from the seed floss – a silky fibre that has been utilised for stuffing pillows, cushions, mattresses, etc. Australian Aboriginal people valued the tree as a fibre resource for making twine. The tree provided useful firewood, while the trunk could be turned into water containers and canoes, or used for making pontoons. The taproot of the young plant is also edible (Brock 1993). The tree has a substantial medicinal reputation. In India the seeds were utilised for treating disorders of the genitourinary tract (gonorrhoea, gleet, chronic cystitis) and the dried young fruit for chronic inflammation of the bladder and kidney, as well as for urinary tract stones. The roots were utilised as a diuretic in Cambodia. The tree yields a gum that has been utilised as an astringent anti-diarrhoeal remedy, as a styptic for haemoptysis associated with tuberculosis or
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menorrhagia (excessive menstrual bleeding), and for treating influenza. The mucilaginous bark was similarly recommended for the treatment of abnormal uterine bleeding, as well as having a reputation as a demulcent and aphrodisiac agent (Kapoor 1990; Burkill 1935). The Mangosteen (Garcinia mangostana) contains xanthones (mangostins) similar to those found in the Mango tree. Mangosteen pericarps have been traditionally utilised in Southeast Asia for treating skin infections and wounds. Extracts, and their component xanthones, have shown diverse pharmacological activities: antibacterial, antifungal, antiretroviral, antiallergic, antioxidant, anti-inflammatory and skin-protective properties. Some xanthones (including mangostins) have been of particular interest as antioxidant and anti-inflammatory agents – suitable for the treatment of some difficult cosmetic conditions including rosacea (a chronic facial condition characterised by redness – i.e. erythema), telangiectasis (dilatation of superficial blood vessels on the face) and to prevent skin ageing. Xanthones also possess central nervous system depressive activity, anti-ulcer potential, and have generated significant interest as experimental anticancer agents against liver, gastric, lung, colon and leukaemia cell lines. Under the name Xango, a Mangosteen juice preparation has recently been marketed as a healthy antioxidant herbal extract (Pinto 2005). Throughout Southeast Asia, Mangosteen rind (sliced and dried) and bark have traditionally been utilised as an astringent remedy for diarrhoeal disorders and dysentery. Externally the fruit rind (pericarp) was applied to atonic (slow-healing) ulcers and swollen (inflamed) tonsils, or was taken for catarrhal disorders of the intestines and genitourinary tract. The astringent attributes of the leaves and bark were also utilised for treating aphthae (an ulcerous
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condition of the mouth), as well as being recommended as a febrifuge (Perry & Metzger 1980; Burkill 1935).
Mangosteen (Garcinia mangostana).
A Valuable Remedy for the Liver and Heart
In the Caribbean, Mango leaf decoctions have been recommended as an antihypertensive remedy. In Curacao, the leaf tea was taken three times daily for three days, although the treatment could be continued indefinitely if required. This use is supported by studies of leaf and stem extracts that have shown hypotensive effects in animals. Mangiferin, and the Mango bark extract Vimang, have good antioxidant and cardioprotective potentials that support these traditional uses – as well as suggesting its value as a supportive remedy for cardiac function. Additionally, Mango extracts can reduce cholesterol levels. In particular, mangiferin has shown anti-hyperlipidaemic and anti-atherogenic properties. In Haiti, Mango bark decoctions were utilised for liver disorders, and mangiferin has shown hepatoprotective and choleretic (increasing bile flow) attributes. The dietary use of the Mango has been associated with a reduced incidence of gallbladder cancer24 (Rodeiro 2008; Pardo-Andreu 2008b; Nair & Shyamala Devi 2006; Prabhu 2006a, 2006b, 2006c; Muruganandan 2005a; Beltrán 2004; Garcia 2003a; Pandey & 24 Investigations have also recently examined the potential of mangiferin in lung cancer and leukaemia (Rajendran 2008a, 2008b, 2008c; Cheng 2007; Peng 2004).
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Shukla 2002; Anila & Vijayalakshmi 2002; Evans 2002; Ross 1999; Oliver-Bever 1986).
Yellow Gentian
Gentiana lutea.
Native to Europe and Asia Minor, Yellow Gentian (Gentiana lutea) has shown radioprotective properties that can be linked to its mangiferin content (Jagetia & Baliga 2005; Jagetia & Venkatesha 2005). This was of interest because extracts of the herb demonstrated an ability to reduce the damaging effects of irradiation on healthy cells without compromising the effect of radiation on malignant cancer cells (Menkovic 2010). Yellow Gentian has long been a component of digestive remedies known as ‘bitters’ which were once highly favoured for the treatment of gastrointestinal disorders. Gentian was particularly valued as an appetite stimulant, for promoting salivary flow, and to facilitate digestion. Its benefits are linked to its ability to promote bile flow (acting as a cholagogue), as well as the secretion of pancreatic enzymes and digestive juices. Improvements in digestive function involve the alleviation of the discomfort associated with dyspepsia, heartburn, nausea and diarrhoea. A ‘Chemist’s Prescription’ in the Western Mail (Perth) of Friday 5 September 1913 recommended: ‘Buy a shilling’s worth of
cascara tincture and get sixpenny worth of gentian root; break the gentian root into small pieces or bruise it as you would bruise ginger; put it int a whisky bottle, fill the whisky bottle nearly full with boiling water and then cork it and shake it well and you will have a good bottle of bitters … If you are not a teetollaer, then put a couple of wineglasses full of brandy or whisky into your gentian root solution to stop it fermenting.’ The extremely bitter tonic prepared from the roots was once even used as a substitute for quinine in malarial conditions. This remarkably bitter property, which is due to a complex of components, persists even when used in great dilutions (1:20,000). Gentiopicroside (2%) has been identified as the main compound responsible for the regulation of gastric secretion, although very small amounts (0.025–0.05%) of another intensely bitter compound (armarogentin), which is 5,000 times more potent than gentiopicroside, is present (van Wyk & Wink 2004; Evans 2002; Weiss 1988). Extracts of the flowers and leaves have demonstrated good antimicrobial (antibacterial, anticandidal) potential, with the components mangiferin, isogentisin and gentiopicrin showing a synergistic activity (Savikin 2009).
Dr. Copp’s White Mountain Bitters advertising card. Publisher: JM Buffords 1883. Digestive ‘bitters’ remedies were reputed to be good for almost anything, as this advertisement indicates. Bitters were as popular in Australia as they were elsewhere, and numerous companies in Melbourne and Sydney manufactured these herbal digestive tonics.
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A Cuban study of the hepatoprotective properties of Vimang, the Mango bark-derived extract, has shown strong antioxidant and hepatoprotective effects. In addition, the chemical structure of mangiferin strongly favours iron chelation – a property that enhances its antioxidant properties. This is of interest because Vimang (and mangiferin) were able to promote the excretion of iron from the liver – which could be very good news for those suffering conditions of excessive iron load such as haemochromatosis25 and β-thalassemia (Pardo-Andreu 2008a, 2007, 2006a, 2006b; Rodríguez 2006; Andreu 2005; Sanchez 2003). Mangiferin may also have protective effects against mercury and cadmium toxicity (Agarwala 2010; Viswanadh 2010; Satish Rao 2009; Dar 2005). Mango bark extracts and Vimang possess analgesic and anti-inflammatory properties that are linked to their polyphenolic components (primarily mangiferin – although catechin, epicatechin, benzoic acid, gallic acid and derivatives are also present). It has shown immunosupportive properties that are of interest for treating immune system dysfunction –such as autoimmune or allergic disorders. Vimang may also have potential for treating endotoxic shock.26 In addition, recent studies have suggested that the antiinflammatory and analgesic attributes of Vimang may be useful for the treatment of neuropathic pain (Garrido-Suárez 2010). In Brazil and India, Mango leaf tea has been taken as a hypoglycaemic remedy for the management of diabetes. An Indian anti-diabetic remedy used dried Mango bark combined in a concentrated decoction with Zanthoxylum armatum, Acacia nilotica and Syzygium cuminii. Some older investigations obtained variable results, with fresh fruit and leaf extracts having hypoglycaemic activity in some investigations, but not in others. However, more recent studies of Mango bark and leaf extracts have shown substantial hypoglycaemic activity that appears to be linked to an effect on pancreatic function, as well as the general blood sugar metabolism (Ojewole 2005; Muruganandan 2005a; Aderibigbe 2001, 1999; Prashanth 2001; Ross 1999; 25 See also chapter 8. 26 De & Chattopadhyay 2009; Lee 2009; Garrido 2006, 2004, 2001; Rivera 2006; Dar 2005; Muruganandan 2005b; Ojewole 2005; Remirez 2005; Garcia 2003a, 2003b, 2002; Martinez 2000; Núñez Sellés 2002; Sanchez 2000.
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Coimbra Teixeira 1998). In addition, mangiferin appears to have a protective effect on renal function in diabetic animals, not only protecting against tissue damage, but also improving renal function (Li 2010; Muruganandan 2002).
Medicinal Salacia Vines
Salacia chinensis is a tropical vine found in northern Australia that ranges to some Pacific Islands, Malesia and Asia. Two other species occur in Australia, both in Queensland – Salacia disepala and S. erythrocarpa.
Mangiferin has been consistently found in the Salacia genus (family Celastraceae) and can be utilised as a marker compound for authentication of herbal drugs such as Salacia oblonga, S. chinensis and S. prinoides. Mangiferin has shown anti-diabetic activity that supports the use of these herbs in diabetes – as well as the Chinese Anemarrhena asphodeloides and the Indian Swertia chirata. These remedies have also shown cardioprotective, renal protective, lipid-lowering and anti-obesity properties that has attracted substantial research interest (Li 2010; Giron 2009; He 2009; Im 2009; Huang 2008, 2006; Suryawanshi 2006; Muruganandan 2005a, 2002; Hoa 2004; Yoshikawa 2002, 2001; Ichiki 1998).
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In addition, Salacia reticulata (roots and stems) is a Sri Lankan herbal medicine that has been utilised for treating liver disorders. Studies determined that its hepatoprotective properties were linked to phenolic components, notably mangiferin and methylepigallocatechin (Yoshikawa 2002).
The Mango Tree as a Biomonitor
The
Medicinal Mango Seeds
The Mango seed kernel is a starchy resource suitable for use as animal fodder although the tannin content imparts an astringent quality and the kernels require soaking before use to facilitate its removal. For culinary purposes, the kernels can be boiled, pickled, or dried Mango kernels and powdered to make flour. In India, the powdered kernel was utilised as an astringent for diarrhoea and bleeding problems (haemorrhage, bleeding haemorrhoids). In addition the kernels, which possess vermifugal attributes, were regarded as being a useful anthelmintic in Nigeria and Gabon (child dose 1–1.5 g powder). Studies have verified this activity, as well as moderate antibacterial and antifungal attributes, and a significant anti-inflammatory action. The anti-diarrhoeal properties of seed extracts were also shown to be significant, with a potent effect on intestinal transit time. However, antimicrobial activity was variable – with extracts being effective against Streptococcus aureus and Proteus vulgaris, but not against Escherichia coli or Klebsiella. Additionally, the kernel has provided a useful remedy for minor cuts, burns, rheumatic pain and asthma. The seed fat has a solid character that resembles coca butter or tallow, and is suitable for use as a coca butter substitute for making chocolates. It has a high stearic acid content that makes it useful for soap making. This fat has also been used for the treatment of stomatitis (mouth inflammation) (Sairam 2003; Ross 1999; Morton 1986; Burkill 1985).
Mango trees in urban settings, Cairns.
The Mango tree has interesting potential as a biomonitor for the detection of air pollution. One Brazilian study isolated large amounts of sulphur, arsenic and copper from leaves in Mango trees growing downwind from a copper smelter in Camacari.27 This posed serious questions regarding potential contamination by these compounds of foodstuffs grown in 27 The monitoring properties of the Guava (Psidium guajava) and the Strawberry Guava (P. cattleyanum) have been similarly evaluated. Guava leaves were shown to accumulate fluorides, sulphur and nitrogen (Moraes 2002).
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the affected area. Soil contamination showed that total acidity and organic carbon content were higher, and the pH-value lower, than was normal. This indicated acidification of the topsoil, which in turn enhanced the availability of copper to growing plants. Interestingly, the functional integrity of the soil was altered. The high sulphur and copper depositions significantly reduced the normal microbial activity and modified the diversity of soil microorganisms present (Klumpp 2003).
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The Anacardiaceae have not only provided delicious fruit and nut resources of international importance, some species have been utilised as fish poisons (piscicides) – another interesting strategy of food procurement. However, in Australia, various other plant classifications were more accessible across the continent and were regularly deployed for this purpose, particularly numerous Acacia species. The chemical basis of their effects was to prove an interesting subject for study due to the great variety of compounds that were discovered to be toxic to fish – but left them fit for human consumption. The Barringtonia genus gained particular repute as ‘fish poison trees’, although a rather surprising array of other native flora were employed in this manner – a number of which also had valuable medicinal attributes.
Chapter 7
FOAMING FISH POISONS compounds has always been a difficult undertaking. The enterprise was made even more complex by the fact that, in the past, many researchers did not appreciate the importance of correct botanical data, which admittedly could be difficult to obtain. A remarkable amount of knowledge was lost simply because of inadequate identification – often due to a paucity of complete plant samples as important details, such as flowers or fruit, could be missing. Wall painting from the Egyptian tomb of Usheret, Thebes, illustrating the ancient art of spear fishing. 18th Dynasty, c. 1430 BC. (Source: Wikipedia)
Knowledge of the effective practical use of the flora was a vital skill in native cultures – for both hunting and healing purposes. Fishing is an ancient method of obtaining food and, while spears and nets rated highly among hunting strategies, the easiest method of all was described by Roth (1901): ‘The simple “muddying” or “puddling” of the water by the feet, in small shallows, and hitting the fish as they come up with a stick, is a procedure common throughout North-West-Central Queensland’. If a very large catch was possible, the deliberate deployment of piscicides (fish poisons or ichthyotoxins) was an option, with the added benefit of avoiding undue exertion and achieving fairly reliable results. Innumerable plants were utilised in this manner, in Australia and around the world. Their selection was usually limited by local availability, with experience in their use leading to some species being favoured over others. Their evaluation was to lead to the recognition of some interesting chemical links with regard to the type of toxins responsible, although the search was not easy. The identification of most plant-based chemical
Two Aboriginal fishermen with spears at the headwaters of the Roper River, Mataranka, Northern Territory. Image by Frank Hurley, between 1910 and 1962. (totallyfreeimages. com) Aboriginal man bark-painting in Umbakumba, Groote Eylandt, N o r t h e r n Territory. Image by Robert Miller 1948. AmericanAustralian Scientific Expedition to Arnhem Land, N o r t h e r n Territory, 1948 (totallyfreeimages.com). 234
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The main subject in the bark painting on the
previous page is a dugong, an important dietary item: ‘This animal is a very favourite article of aboriginal diet. It feeds on marine vegetation and yields a large quantity of oil. Being a mammal and suckling its young, it is supposed by some to be the origin of the sailors’ myth of the mermaid. An old natural history book informs us that “its oil has similar qualities to cod liver oil, having been used successfully in some cases of consumption”’ (MacPherson 1930). Today dugongs are under threat, a highly vulnerable species with a low birthrate whose environment is plagued by marine pollution and habitat modification. They can live for 70 years, although few would reach such an age. Australia has the largest protected dugong refuge in the world – although these mammals are still not entirely safe from hunting, marine accidents, and being tangled in fishing nets.
Dugong oil entry from British Pharmacopoeia, 1867.
Difficulties with Plant Identification
Duyfken replica on the Swan River. This Dutch ship, captained by Willem Janszoon, charted the shores of Cape York Peninsula in 1606 – setting out from the port of Bantam (now Banten, in western Java) and making landfall at the Pennefather River in the Gulf of Carpentaria. This was the first true European authentication of the great, and mysterious, southern continent. Janszoon mapped over 200 miles (300 km) of the Australian coastline, although he believed that Cape York was a southern extension of New Guinea, or Nueva Guinea, as it was then marked on the maps. (Image courtesy: nachoman-au, CC-by-SA 3.0)
Pennefather River. (Courtesy: Katrin Holmsten)
In 1916 the Australian researchers Ronald HamlynHarris and Frank Smith published an influential paper entitled On Fish Poisoning and Poisons Employed among the Aborigines of Queensland. This study offers an insight into the difficulty of obtaining good quality botanical samples and their investigation. Sometimes insufficient quantities of plant material were available, while at other times the specimens collected were incomplete. For example, a rainforest vine from the Pennefather River, Queensland, yielded a rapid and effective poison which was called ‘nero’. Unfortunately, the vine flowered and fruited in the wet season, a time when its swampy habitat was largely inaccessible, and obtaining specimens was thus an exercise fraught with difficulty. The Reverend N. Hey stated: ‘This fish poison is used only in salt or brackish water in conjunction with plentiful supplies of green-ants’ nests [Oecophylla smaragdina] which are calculated to tempt fish to the surface and when they are stupefied, they are most easily caught’ (cited in Hamlyn-Harris & Smith 1916). The manner in which the poison was utilised was ingenious. The vine was beaten out and coiled in lengths around staves, which were then pounded together under the water to disseminate the poison. Experiments verified ‘the great effectivity of the prepared plant: the Green ant nest.
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fish are rapidly paralysed and killed’. The vine was probably from the Derris genus but, because many rainforest lianas are virtually impossible to distinguish from each other, the exact species providing the drug cannot be established with certainty – especially one hundred years after the event. Records regarding a shrub from Dorothy Creek (Katherine River) in the Northern Territory are equally interesting. Samples were supplied to the researchers by a Mr RH Teck-Brook who wrote: ‘As far as I can see, the shrub has no seed, and I can find no trace of seed of any kind. It is about four to five feet high, and the blacks scrape the bark off with a sharp stone and either pound it on another stone and then push it into the water, or else, after pounding and bruising the bark, they put it in a grass basket and drag the basket with the pounded bark inside through the water and in five minutes the fish are floating on the top.’ Experimentally, the infusion ‘proved innocuous to test fish’. Possibly the plant needed to be utilised fresh, or the method of preparation may have influenced the results. Other factors could have played a role: the time of collection may have been important, as seasonal influences often modify the level of active chemical principles, or the active compounds may have been unstable and dissipated with processing or storage. The investigation of another fish poison was similarly hampered by incomplete data. Mr JL Bramford of Oaklands (via Cairns) provided details: ‘the material is placed in waterholes overnight and fish are found dead on the surface next morning. The natives of the district also employ it as a stimulating or perhaps sedative medicine’. The following somewhat disturbing observation was made: ‘Mr Bramford is of the opinion that its use accounts for the death of many small children, the infants pining away when the opiate (?) is indulged in by the mothers, who are with difficulty induced to abandon the habit.’ There is no real idea of the plant’s identity, although its apparent sedative activity is intriguing. Experimentally it was found to be a slow, but effective, fish poison.
Bush Poisons
Fish poison resources were diverse, ranging across many plant families and genera. Their level of toxicity was equally varied. Some were toxic to fish only, while
Wild Passionfruit (Passiflora foetida). The green fruit of this naturalised Passionfruit vine is considered to be poisonous, and the leaves and stems have been used for fish poisoning purposes in the Northern Territory. When ripe, the small fruits turn yellow and are then considered edible (Lindsay 2001).
others were also poisonous to man and/or animals (particularly stock). Many had a medicinal reputation. An understanding of the chemistry involved was to provide explanations for some of the discrepancies in these effects. There are differences in the toxic reactions that occur in cold-blooded and warm-blooded animals – and substantial variations in reactions can occur with changes in dosage or route of administration. In addition, the rate of metabolism of a toxin and the method of its excretion provide other clues for solving toxic puzzles. Fish poisons were among the first native plants to truly intrigue chemists. Many piscicidal plants contained saponins – compounds characterised by an ability to produce a soapy foam when mixed with water (Latin sapo means ‘soap’). Saponins, however, were not always the answer to the toxicology puzzles. Tannin was one of the less potent components of fish poison plants. Usually it was a slow-acting piscicide that was, nonetheless, effective. A number The bark of the White Apple (Syzygium forte subsp. potamophilum) has been utilised as a fish poison in the Northern Territory. This tree can be used to fashion dugout canoes, and the timber is an extremely useful firewood resource (Marrfurra 1995). (Image courtesy: Russell Cumming, flickr)
FOAMING FISH POISONS
of Eucalypts fall into this chemical category, including the Coolibah (Eucalyptus microtheca). Walter Roth provided details of its deployment: ‘numerous leafy boughs and branches of “gum tree” (Mitakoodi, joo-a-ro) are utilised … The whole camp of blacks working at it, will start throwing these in first thing in the morning; during the day the water becomes darker and darker and strongly-smelling until by the following morning at sunrise when it is almost black, the fish all lie panting at the surface and are easily caught’ (Roth 1901). Various tannin-containing Terminalia species were utilised similarly: T. laurinoides, T. tomentosa and the Damson (T. sericocarpa) – although considered less effective, they nevertheless produced ‘death in sufficient concentration’ (Hamlyn-Harris & Smith 1916). Len Webb commented that ‘a toxic principle other than tannin, of which 8 per cent. was present, could be demonstrated’. In India, Terminalia bellerica fruit was used similarly: ‘the rind of the fruits is rich in tannin … Cases of narcotic poisoning in humans by the kernels were reported … It is a fish poison and the fruit contain 5-17 per cent. tannin’. Other tannin-rich species included Terminalia catappa (bark) and T. chebula (fruit) (Webb 1948). Another species of toxicological interest is Terminalia oblongata (Yellow Wood) which contains a couple of potent toxins, punicalagiin and terminalin.1 This species, which has a very high tannin content (20–29%), has been responsible for poisoning sheep and cattle in Queensland (Oelrichs 1994; Webb 1948). 1
Damson bark, Te r m i n a l i a sericocarpa.
1 The unrelated rainforest tree Flindersia xanthoxyla has also been known as Yellow Wood, although it presents no toxicological concerns.
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Bitterbark: Medicine and Poison The Bitterbark tree (Alstonia constricta) contains a thick milky latex with therapeutic properties, notably as a febrifuge. Len Webb commented that it was ‘claimed Alstonia constricta bark. to be a deadly (Courtesy: Ethel Aardvark, poison. Latex used Wikipedia) to cure infectious sores, although very severe on the skin [Woorabinda, Queensland]’ (Webb 1969). There is no doubt that the tree has poisonous potential. In northern Queensland, at Mossman Gorge, the milky sap from the pounded bark was used to stupefy fish (Roberts, Fisher & Gibson 1995). Selwyn Everist mentioned that ‘Bitter Bark’, which had an intensely bitter taste and contained a number of alkaloids (notably echitamine and alstonine), was responsible for incidents of stock poisoning that involved central nervous system dysfunction. Of the Milkwood (Alstonia actinophylla), Dulcie Levitt mentioned its use also for treating sores, despite some toxic potential: ‘the thick corky bark was chipped with a piece of stick until the milky sap oozed out. This was collected on a twig and applied to small sores. Care was taken not to get it on the fingers because if it got into the eyes it could cause blindness.’
A Worldwide Diversity of Fish Poison Plants
The Cherry Beech (Ternstroemia cherryi) is a small tree of the rainforest understorey that produces an oval yellow fruit which splits open to reveal attractive bright pink-red
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arils. This edible fruit ‘does not taste badly’ (Flecker 1948). However, the bark had a good reputation a fish poison and was pre-heated in hot ashes before use. Citing HamlynHarris & Smith (1916), Len Webb (1948) noted: ‘Tests showed that it was a highly efficient and rapid fish poison, the bark being more effective than the leaves. The plant is highly sapotoxic’. In Papua New Guinea, the entire plant was considered to be poisonous to humans, dogs, pigs and fish, although the fruit could be scraped and placed onto a sore or cut to facilitate healing (Woodley 1991). Bark from a couple of other species have been used in the Philippines and Indonesia as arrow and fish poisons (Perry & Metzger 1981; Burkill 1935). Overall, Ternstroemia has been considered to possess little medicinal value. Ternstroemia gymnanthera leaves were used by mountain people in Taiwan to allay the symptoms of malaria, and the bark, which was considered to possess astringent properties, provided an antidysenteric remedy. The toxic reputation of the genus, however, would advise caution. Another fish poison of interest is the Water Pepper, Polygonum hydropiper, a herb of damp and marshy places.
Ternstroemia cherryi, the Cherry Beech, is the only Australian member of the Camellia family (Theaceae) and is therefore related to the Tea plant (Camellia sinensis). Originally, because it was thought to be more closely allied to the Mangosteen (Garcinia mangostana), it was classified as Garcinia cherryi. (Lower image courtesy: David Tng, florafnq.wordpress.com)
Tom Petrie mentioned its use as a fish poison around Brisbane, noting that it was pounded up with sticks and thrown into the water, which was then stirred up with the feet. Similar uses of related species, including Polygonum orientale, P. strigosum and P. minus were recorded. Hamlyn-Harris & Smith (1916) concluded that ‘[a] somewhat concentrated infusion the Polygonum spp. tested proved efficient stupefacients; the fins and tails became contracted and depressed, and death has been known to follow within 4½ hours. P. hydropiper proved most effective, stupefaction being pronounced in a period of 4 hours’. The herb contains diverse chemical components. The bitter flavonoid rutin is present, as well as the spicy pepper-like compounds polygodial and warburganal, which impart a pungent character to the plant. It is the polygodial component that has shown strong piscicidal activity (Harada 1994).
Polygonum hydropiper and P. tomentosum, from Bilder ur Nordens Flora (published between 1901–1926) by Carl Axel Magnus Lindman, Professor of Botany at Swedish Museum of Natural History, Stockholm.
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A Worldwide Diversity of Fish Poiison Plants
An enormous variety of plants have been used as piscicides (ichthyotoxins) and they contain a substantial diversity of effective chemical components. While fish poisons sourced from the Fabaceae family, notably the rotenone-containing vines Lonchocarpus and Derris, are among the most familiar that are deployed around the world, the following species are illustrative of the great range of compounds that have been discovered (Harada 1994): • juglone from Juglans mandshurica (Juglancaeceae): roots and fruits used in Japan. • justicins from Justicia hayatai var. decumbens (Acanthaceae): whole plant used in Taiwan. • callicarpone from Callicarpa candicans (Verbenaceae): leaves used in Caroline and Philippine islands. • huratoxin from Hura crepitans (Euphorbiaceae): latex used in South America. • vibsanine A from Viburnum awabuki
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(Caprifoliaceae): leaves used in Okinawa, Japan. • inophyllolide from Calophyllum inophyllum (Guttiferae): leaves and seeds employed on Malay Peninsula. • ichthyotereol from Ichthyothere terminalis (Compositae): leaves used in the Amazon. Chemical investigations have therefore confirmed the potent effects of many species, some of which are found in Australia – that is, Calophyllum inophyllum and Callicarpa candicans. Occasionally these discoveries have suggested additional pesticidal or herbicidal potential. For instance, studies determined that while α-naphthoquinone from the shoots of the aquatic weed Ammannia baccifera (Lythraceae) showed only mild piscicidal activity, it later attracted interest as a natural herbicide for killing weeds in rice paddy fields. This herb is native to Western Australia, the Northern Territory and Queensland.
A Frothy Tale
The frothy (soapy) effects of saponin-containing plants have been familiar to many cultures. The 1948 edition of American Pharmacy provides details of their activity: Saponins when shaken with water form colloidal solutions and a stable froth is formed similar to that of soap, hence their name. They are true emulsifiers in that they form a coherent film around the oil globules and are powerful surface active agents [surfactants] in that they lower interfacial tension greatly … The tincture is usually placed in a dry bottle and the oil added to it in portions with vigorous agitation after each addition. Saponin emulsions are fine grained and stable. They are not very viscous, however, and as a result cream [forms] readily unless some gum or other agent is added to increase the viscosity. They are stable to alcohol and acids and are not subject to decomposition (Lyman 1948).
Blood Flower or Fireball Lily bulbs (Scadoxus multiflorus subsp. katerinae, pictured here, and S. cinnabarinus), the Mammy Apple (Mammea africana), Cashew Nut (Anacardium occidentale), and West African Ebony (Diospyros mespiliformis) are among the familiar species utilised as fish poisons.
Saponins are found in a remarkably wide range of plants. Although these compounds are poisonous to cold-blooded animals (e.g. fish and snails), their toxicity decreases greatly in warm-blooded animals. Fortunately, in humans saponins are destroyed by the stomach enzymes. In addition, they are not well absorbed because they bind to food components,
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which facilitates their excretion from the digestive system. However, the fact that these water-soluble compounds are readily absorbed by fish allows them to act quickly to paralyse respiratory function, resulting in suffocation. It is thus no surprise to find that many fish poison (piscicidal) plants contain saponins. It is this difference in the absorption and processing of these chemicals that can explain the somewhat unexpected medicinal uses of the various saponincontaining plants. The recommendations found in the 1941 Martindale Extra Pharmacopoeia for Soapbark, sourced from the South American tree Quillaja saponaria, are illustrative of both the toxic and medicinal reputations of saponin-containing plants: ‘Quillaia [sic] (Panama Bark, Soap Bark): The dried inner part of the bark of Quillaja Saponaria and other species (Rosaceae).2 Contains quillaic acid … and sapotoxin … closely allied to saponin. Has a sweetish but acrid aftertaste and possesses emulsifying properties, causing frothing in water in which it has been macerated. Its lather kills pediculi of scalp. Soapbark has been used as an expectorant in bronchitis; is contraindicated in inflammation of the intestines or stomach, or ulcerated condition of the mucous membrane. The powdered bark is a powerful sternutatory [induces sneezing].’ Quillaja saponaria originates from Chile, although it has been cultivated for medicinal use in India. Quillaja possesses a wide range of pharmacological properties – among them astringent, anti-inflammatory, antimicrobial, cytotoxic, cholesterol-lowering, expectorant, haemolytic and immunostimulant actions. Lyman, in American Pharmacy (1948), gives further details regarding the pharmacological value of saponincontaining herbs: The most commonly used drugs containing saponins are quillaja bark, sarsaparilla, and senega root. The tincture is the preparation principally used. Quillaja is used much more frequently than senega because it has a less unpleasant taste and a lesser therapeutic action. Due to the irritating property of the saponins they are never used for emulsions which are to come in contact with mucous membranes. They also have an extremely acrid taste which provokes a flow of saliva, nausea, vomiting, and diarrhoea. Saponins also cause haemolysis [breakdown or 2 This tree, which is now placed in the Quillajaceae family, is also an effective fish poison.
Quillaiae cortex from Peter Squires, Companion to the latest edition of the British Pharmacopoeia, comparing the strength of its various preparations with those of the United States, and other Foreign Pharmacopoeias, to which are added Not Official Preparations and Practical Hints on Prescribing. London, 1899. destruction] of the red blood cells, because of their affinity for lipoids, but as these compounds are not absorbed, this toxicity is apparent only upon intravenous injection. Their chief toxicity is due to their local irritation on mucous membranes.
While the haemolytic properties of these herbs are not normally evident, gastrointestinal injuries such as ulceration increase the risk of saponin absorption, which can lead to internal bleeding. If injected directly into the bloodstream saponin exposure can be fatal. This is, however, unlikely to happen under normal circumstances, and injectable strategies would only be utilised in experimental situations.3 3 It should be noted that haemolytic activity is not restricted to saponins. Therefore, at times the chemical analysis of a plant extract can become quite complex, particularly when testing for haemolytic activity – which can be positive without the presence of saponins.
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Quillaja saponaria, from Koehler’s Medicinal Plants, 1897.
Immunomodulatory Adjuvants
Immunomodulatory properties can make an important contribution to the efficacy of some saponin-containing herbs. During the 1920s Quillaja attracted a great deal of research interest when the herb was shown to substantially enhance immune responses. Studies on Quillaja saponins isolated from the bark revealed immunepotentiating activities with the potential for pharmaceutical development. Quillaja saponins were found to be eminently suitable for use in vaccine formulations as adjuvants – substances that play an essential part in triggering the immune response of a vaccine mixture. Adjuvants act to potentiate the effects of the preparation without 4 Some controversy surrounds the toxic potential of adjuvants. Aluminium salts, which are widely utilised, can cause neuron cell death and have a possible link to Alzheimer’s disease. Experimental evidence exists for squalene having a potentiating effect on arthritis, while oil–water suspensions have been linked to autoimmune system problems in animal studies.
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having any toxic effects.4 Thus the manner in which a saponin stimulates the immune system is important, as it not only influences the immune response but can also alter the protective efficacy of the vaccine itself. The fact that Quillaja saponins have antiviral activity against a variety of viral agents is of interest for drug development purposes for use in HIV vaccines. Quillaja saponins have provided adjuvants for use in animal vaccines for control of infectious diseases such as canine kala-azar (due to Leishmania donovani parasites), or tick-induced Lyme disease. Its potential for use in human vaccines continues to be investigated, with success in numerous clinical trials – notably for incorporation into vaccines for malaria, hepatitis and cancer (breast, melanoma, small cell lung and prostate cancers). There are, however, dose limitations due to side-effects – including the haemolytic activity characteristic of saponin compounds when used in an injectable form. These saponins have a complex chemical structure, and it has been difficult to unravel which of the components possess the best adjuvant activity. Research has focused on a purified saponin fraction (QS, notably QS21 and Quil A), although there are problems with chemical variability and stability of the saponin, as well as difficulties in supply and extraction of the raw material (Adams 2010; Kensil & Kammer 2010; Borja-Cabrera 2002; Kamstrup 2000; Marciani 2000; Jiang 1999; Johansson 1999; Kensil 1998; Dotsika 1997; Sjolander 1997, 1996; So 1997). Despite the complexities, some innovative therapeutic advances have resulted from the search. Modified forms of Quillaja saponins have been used to promote the absorption of insulin and antibiotics via ocular and nasal administration, and to enhance the intestinal absorption of various other compounds. Other applications include the facilitation of cholesterol solubility, which could be useful for pharmaceutical manufacturing strategies (Mitra 2001; Chao 1998; Pillion 1996; Recchia 1995). Quillaja saponins can modulate microbial growth in fermentation procedures. The effect (promotion or inhibition) depends on the type of saponin used and the concentration used (Sen 1998).
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There are a number of saponin-containing herbs with similar immunomodulatory and adjuvant potential. Tomatine from the tomato plant (see chapter 4) has shown immunopotentiating properties and has been proposed as an adjuvant for a malaria vaccine (Heal 2010). Panax ginseng has shown a potentiating action in aluminium hydroxide-adjuvanted vaccines (Rivera 2003). Other saponin-containing plants that have been suggested as adjuvant resources are illustrative of the great diversity of these compounds that are available: Panax notoginseng (notoginsenosides, ginsenosides), Platycodon grandiflorum (platycodins, platycoside E), Polygala tenuifolia (onjisaponins, plygalasaponins, tenuifolisaponins), Glycyrrhiza glabra or Liquorice (glycyrrhiza saponins), Glycine max or Soya beans (soyasaponins) (Sun 2009).
Calliandra pulcherrima, from Flore des serres et des jardins de l’Europe by Charles Lemaire and others, Louis van Houtte, Ghent, 1845. A triterpenoid saponin (pulcherrimasaponin) with immunomodulatory activity has been isolated from Calliandra pulcherrima leaf extracts. This compound showed potential as a vaccine adjuvant due to its similarity to the Quillaja saponin (QS21) from Quillaja saponaria (Silva 2005).
A Native Foambark The flowers of the Foambark (Jagera pseudorhus), which have a heavy, sweet fragrance, are a good nectar resource for bees. They are highly attractive to many pollinating insects in the tropical rainforest – wasps, ants, beetles and flies. The Foambark is a small native rainforest tree found growing along riverbanks and in the lowland forests of Queensland and northern New South Wales, extending to Papua New Guinea.
Foambark (Jagera pseudorhus, formerly Cupania pseudorhus) provides an example of a native saponincontaining plant that once achieved a limited measure of commercial value. The saponin component explained its use as a popular Aboriginal fish poison. Mr JM Kenny of Hull River described the manner of its preparation: ‘The bark is carefully scraped from the tree trunks and limbs and cooked in native ovens for about half an hour; then when taken and put into a
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pond and well mixed in the water still held in dilly bags, soon acts on the fish’ (Hamlyn-Harris & Smith 1916). It had a rapid and powerful action, producing excitement, stupefaction and paralysis. In concentrations as low as 1:1,000 death occurred in less than an hour. Foambark was used domestically during the First World War as a substitute for Soap Tree – Quillaia or Quillaja – bark. In particular it was useful for producing the foamy ‘head’ characteristic of beer and some cordials. In the early 1900s around nine tons was collected and distributed to Australian manufacturers and brewers, largely due to the efforts of Queensland Forestry officials. However, the scattered distribution of the tree made collection efforts difficult and costly. This proved to be a significant obstacle to obtaining a reliable supply of the raw material and establishing a market. In addition, later reservations with regard to the toxicity of the saponin played a part in discouraging its use. Experiments had shown that the haemolytic activity of the bark was very close to the level that was used for ‘foaming’ purposes – i.e. haemolysis of blood cells occurred at dilutions of 1:14,000, while frothing was induced at 1:10,000 (Francis 1929). These concerns were similar to those held regarding the use of Quillaja bark due to its saponin content and potential absorption via skin injuries or internally in conditions associated with mucous membrane damage.
There are two species of Foambark found in tropical Australia other than Jagera pseudorhus. Shown here is J. javanica subsp. australiana (listed as vulnerable); the other is J. dasyantha, the distribution of which extends to Papua New Guinea.
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Ackee: A Toxic Tropical Fruit
Blighia sapida is a saponin-containing fruit tree of the Soapbush family (Sapindaceae), native to tropical West Africa and now found in many other parts of the tropics. It was named for Captain Bligh of HMS Bounty fame – although considering the tree’s poisonous reputation he may not have been too impressed by the honour.
The unripe fruit or the scarlet rind of the Ackee (Blighia sapida) has provided a fish poison in Cuba, Jamaica and the Ivory Coast. This species has been widely planted in the tropics, including Australia, for its ornamental fruit – despite the unripe fruit’s serious toxic potential.
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The bell-shaped fruit of the Ackee (or Akee) has a distinctive thick, leathery scarlet rind. The shiny black seeds within are surrounded by a thickened creamy edible aril. The rind contains a saponin, and the green fruit can be lathered in water (or burnt and ashed) for use as a soap. Blighia unijugata (leaves, flowers, fruit or twigs) were used similarly in Ghana. The Ackee tree gained a notorious reputation due to annual outbreaks of poisoning (‘vomiting sickness’) associated with its use, particularly in the West Indies. Here the introduced tree yields a fruit crop that has become an important export for Jamaica. It is the seeds, and the unripe fruit, that are toxic. Even squirrels know to leave the seeds alone – they burrow into the fruit and eat the ripe aril, but are wise enough to leave the rest untouched. The fruit should not be used until it has ‘yawned’ (i.e. fully ripened and split open), a natural process that exposes the contents to light and results in a drastic reduction (around 90–95%) in toxicity. The tasty aril can then be parboiled or lightly fried for use in stews or casseroles. Many incidents of toxicity have resulted from collection of the partially ripe unopened fruit or the use of arils containing undeveloped seed remnants. Between 1886 and 1950 at least 5000 deaths were attributed to Ackee poisoning. Fatalities continue to be incurred. An incident during May and June of 1984, in Côte d’Ivoire, saw forty starving children die from eating the fruit. Formerly, it was thought that the membrane attaching the aril to the jacket contained the toxin, or that the over-ripe arils were responsible. Later, when this was found to be incorrect, food preparation techniques could accurately avoid the toxic components. The compounds implicated were eventually identified as hypoglycins – the unripe aril and seeds contain hypoglycin A, with the somewhat less toxic compound hypoglycin B also being found in the seeds. Hypoglycins have
a strong emetic property, as well as a serious hypoglycaemic action that is complicated by the fact that it is a delayed effect. Symptoms involve the sudden onset of vomiting, which eventually ceases, and the person becomes drowsy or sleeps. However, the vomiting begins again and this, if unalleviated, leads to dehydration characterised by exhaustion and prostration; the person later becomes comatose and fatalities result (Ken 1998; Singh 1992, Melville & Addae 1988; Foungbe 1986; Morton 1986; Sherratt 1986; Ayensu 1978). The Ackee has had a few medicinal uses, some of which appear to be quite inadvisable – for example, small doses of a seed extract used as a vermifuge. In Brazil this treatment was accompanied by the use of a purgative to remove the intestinal worms. Less daunting was a Cuban recipe that blended the ripe arils with sugar and Cinnamon as a febrifuge or dysentery remedy (A cologne has also been prepared from Ackee flowers in Cuba.) In Colombia, the leaf and bark were considered to have stomachic properties. Other recommendations have included its use for yellow fever and epilepsy. The bark of the tree, mixed with aromatic spices, provided an analgesic ointment in Côte d’Ivoire, while the crushed new foliage was applied to the forehead to ease severe headaches. Pulverised, the bark was ground with hot chillies and rubbed over the body as a stimulant in Ghana. The bark pulp has been used as a remedy for oedema, intercostal pain and orchitis (testicular inflammation). In Côte d’Ivoire a salted leaf poultice was applied to the ulcers of yaws, while the leaf juice provided eye drops for use in ophthalmia and conjunctivitis. The closely related Blighia unijugata was used therapeutically in Ghana – the bark pulp as a purgative or for fevers; the root as a styptic (to reduce bleeding during childbirth); the seeds as an emetic; or the leaf pulp rubbed on the body as a strengthening and relaxing medicine (Morton 1986; Ayensu 1978).
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Medicinal ‘Bush Soaps’ The Indian Soap Nut
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of the wet season, when the water source would be quickly washed out and replenished. The bark was once proposed as a possible substitute for Quillaja bark as a foaming agent but tests undertaken by the Queensland Department of Agriculture and Stock between 1917 and 1918 established that it would not be suitable.
Australian Alphitonia
The Soap-nut tree (Sapindus mukorossi) of northern India.
The genus Sapindus (family Sapindaceae) contains a number of trees that have been utilised around the world as a source of cleaning products. The Indian Soap-nut tree, a native of the Himalayas, Japan and China, is also a well-known fish poison. The pods were valued for soap production in China and northern India, and it has provided a useful shampoo that can eradicate hair lice. Soapnut products were generally believed to beautify the skin and were even reputed to remove freckles. Medicinally, the fruit decoction, which had an expectorant action, has been employed for treating excessive salivation, and for chlorosis (chronic iron deficiency anaemia) (Burkill 1935). The Australian Soap Tree or Red Ash (Alphitonia excelsa) is another native species with a soapy reputation. The foaming properties of the leaf saponins made it a popular ‘bush soap’. Children rubbed the leaves on their hands to remove the ink stains inevitably associated with dipping steel-nibbed pens in inkwells. The tree has been employed as a fish poison – the red-black berries and leaves were crushed and added to water. Although it could be utilised throughout the year, the poison was said to be most potent when the tree was in fruit. There was a bit of a problem with the use of this toxin, however, as it rendered the water undrinkable, and thus it was used only in times of great need, or at the beginning
Soap Tree (Alphitonia excelsa).
The Alphitonia genus is quite small and mainly of tropical Australian origins – although a few species can be found in Oceania. There are five Australian species: A. excelsa, A. oblata, A. petriei, A. pomaderroides and A. whitei. There has been a bit of confusion in the botanical literature – Alphitonia incana. Alphitonia oblata is referred to in some older texts as both A. incana and A. philippensis, neither of which is found in Australia. In addition, the variety formerly known as Alphitonia obtusifolia var. tenuis has been reclassified as A. pomaderroides.
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The Soap Tree or Red Ash (Alphitonia excelsa) is perhaps the most familiar of the genus. While it usually favours a riverine habitat, it can extend its distribution into drier areas. This species also found in Southeast Asia and Papua New Guinea. The leaves are quite distinctive, as the Reverend Tenison-Woods commented in his Botanical Notes on Queensland – The Forests or Scrubs (1882), and have been used as a flavour enhancer in bush cooking, wrapped around food: Occasionally through all the Brigalow one meets with trees of Alphitonia excelsa, a member of an order (Rhamnaceae) not at all well represented in this part of Australia. It may be easily known at a distance by its dappled aspect, for the oval leaves are a bright shining green on one side and white underneath, and thus it always has a speckled appearance. Like the sandal wood it is very wide spread, and is as common in the dense tropical jungle as in the desert. This feature is quite exceptional, for there is little else common to the two floras.
In addition to its useful soapy attributes, Red Ash timber is hard and durable. It was used for the manufacture of weapons such as the flat woomera used for fishing and fighting. Joseph Maiden (1895) commented: ‘Although not one of our commonest timbers, I draw attention to this timber because of the peculiarity of its colouring. When the log is first cut, it resembles ordinary ash in colour, and for some time no change is perceptible. After a time it gradually assumes a reddish colour, which deepens for two or three years, by which time it has assumed a fiery red appearance. This colouration is superficial, and may be removed by the plane, but its depth of tint again returns in process of time. It is very ornamental.’ Woomera drawing, circa 1867 by George Gordon McCrae. (totallyfreeimages.com)
The leaves of the Red Ash (Alphitonia excelsa) have been widely deployed as a ‘bush’ detergent. They also possessed good antiseptic properties. The soapy lotion was popularly applied to treat minor skin problems such as sores, ringworm or boils (Barr 1988). The leaves even provided a useful anti-inflammatory remedy for sore eyes. The young leaf tips could be chewed and the juice swallowed to ease an upset stomach, a remedy that was said to act very quickly (within 5–10 minutes). It was equally useful for the relief of diarrhoea (Kyriazis nd). An analgesic liniment has been prepared from the root and wood, which was employed for the relief of body pain including rheumatic and arthritic pain. The closely related White or Pink Ash (Alphitonia petriei) was employed in a similar manner. Bathing the head with a warm leaf infusion was said to be good for headaches, while a decoction of bark and wood was gargled to ease toothache (Cribb & Cribb 1981; Webb 1969). The bark has a strong liniment-like aroma that has been likened to Sarsaparilla. This is possibly due to methyl salicylate (or a closely related compound) – which is responsible for the familiar scent of Wintergreen oil, a stimulating aromatic (minty-fragranced) liniment. Methyl salicylate is the active component of products such as Mentholatum Deep Heating Rub that are used for the relief of aches and pains including sprains and arthritic inflammation. In Papua New Guinea Alphitonia ferruginea, which was similarly employed, was noted to contain methyl salicylate (Woodley 1991). Little else appears to be known regarding the chemistry of the genus. Alphitonia zizyphoides, which is distributed from Sumatra and the Philippines to Polynesia, has likewise had diverse medicinal uses in Oceania (see Table 7.1). Investigations of Samoan-sourced samples yielded saponins (zizyphoides), as well as a unique anti-inflammatory compound (Li 1994; Cox 1993).
Alphitonia petriei: tree trunk. (Courtesy: Peter Woodard)
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(Right) The White Ash (Alphitonia petriei) is an endemic species that ranges from Queensland into northern New South Wales. The plant was originally collected near Kuranda (Cairns), and named in 1925 in honour of WR Petrie, who had noticed its distinctive botanical characteristics.
(Left) The Australian Red Almond (Alphitonia whitei) has an antiseptic bark useful for treating skin sores. Its pungent aroma was also said to clear head congestion.
Table 7.1 Medicinal Alphitonia
There are around 10–20 species (estimates differ substantially) in the genus Alphitonia, with around five being found in Australia. A number have been utilised in the herbal traditions of Southeast Asia (Borneo, Malaysia, Indonesia) and the Pacific Islands, a few of which are endemic species, such as Alphitonia ponderosa from Hawaii, and A. marquesensis from the Marquesas Islands, French Polynesia. Species (distribution) Alphitonia franguloides Fijia, endemic
Alphitonia moluccana (syn. A. incana) Indonesia, Malaysia, Philippines, China
Alphitonia neocaledonica New Caledonia, endemic Alphitonia philippensis Philippines Alphitonia zizyphoides Pacific Islands: American Samoa, Cook Islands, Fiji, French Polynesia, New Caledonia, Niue, Tonga, Vanuatu, Wallis and Fortuna Islands
Traditional recommendations (source) Fiji (Weiner 1985): Inner bark of species known as Doidamu used as a remedy for treating ‘relapsing illness’ following childbirth. Useful for joint pains in the hip, as well as headaches. Amboina and Indonesia (Perry & Metzger 1981; Burkill 1935): Bark: chewed to clear the throat and enhance the voice for singing festivals. Papua New Guinea (Perry & Metzger 1981; Stopp 1963): Bark: applied to non-infected skin swellings. Leaves: utilised as a wrapping for corpses and considered to be an excellent choice for bearing the forces of death. New Caledonia (Lin 1995): Used for the treatment of rheumatism, dermatosis (skin disorders), and to ease childbirth. Leaf: extracts contain numerous flavonoids. Philippines (Perry & Metzger 1981): Bark: chewed and the saliva swallowed to cure coughs and ease stomach troubles. Pacific Islands (Agroforestry database, www.worldagroforestry.org): The bark, often in combination with other species, is used for treatment of stomach ache, constipation, coughs, headaches, menstrual pain, and prolapsed rectum in postpartum women. The sap is used to treat earache, swelling, fever, and cancer. A phenolic compound in the bark, alphitol, has been shown to have anti-inflammatory activity. Apiculture: The species is reportedly a good source of nectar for bees. Tonga (Whistler 1992a, 1992b): Taken to ease stomach ache. Incorporated into a remedy for postpartum women to treat rectal prolapse. Pacific Islands (Cambie & Brewis 1997): Fiji: bark scrapings decocted and taken daily (with other plants) as a remedy for infertility. Vanuatu: stem juice was reputed to have abortive effects. Pacific Islands (Weiner 1985): Tahiti: used to make a lotion for skin problems such as eczema. Tonga: bark decoction used as a remedy for constipation, coughs, headache, and menstrual pain. Fiji (known as Kalevu): employed for treating ‘sickness in the bones’. Fiji (known as Doi, i.e. A. zizyphoides): liquid pressed from the leaves was taken for blood in the urine (haematuria). Fluid from the inner bark recommended for high blood pressure (a feeling of ‘insects crawling under the skin’) and severe headache.
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A Rainforest ‘Potato Vine’
In the Queensland wet tropics the October Glory vine (Faradaya splendida) was used as a seasonal ‘calendar plant’ by Aboriginal people. When the flowers appeared the scrub turkey (Alectura lathami) was ready to lay eggs. Later, when the potato-like fruit began falling off the vine, it was time to visit the turkey mounds to harvest the eggs.
The lovely Faradaya splendida is a rainforest liana of northern Australia and Papua New Guinea that flowers with glorious displays of masses of pristine white blossoms. In 1878 the Government Botanist FM Bailey wrote of its beauty: ‘Faradaya splendida, F.v.M., a Verbenaceous rampant climber, bearing large white flowers, is thought by some the handsomest climber of the north. It usually flowers about September and October.’ The plant has been known as the Potato Vine due to the characteristic ‘potato fruit’. Despite a watery consistency it is edible, albeit reputed to have a rather poor flavour, and is rated as a rather lacklustre bush food. A large seed occupies the major portion of the fruit, leaving little room for flesh, which is easily pitted and bruised when it falls from the vine.
In the early 1900s EJ Banfield, a long time resident of Dunk Island (140 kilometres south of Cairns), mentioned its use as a piscicide: ‘Portions of the vine are cut into foot lengths, the outer layer of the bark is removed and rejected, and the middle layer alone being preserved. This is carefully scraped off and made up in shapely little piles on fresh green leaves. When a sufficiency is obtained it is rubbed onto a stone previously heated by fire. The stones being then thrown into a creek or a little lagoon left by the receding tide, the poison becomes disseminated, with fatal results to all fish and other marine animals’ (Hamlyn-Harris & Smith 1916). Experiments isolated a saponin as the active principle and verified the potent fish poisoning effects of the vine. There are a couple of related species that have been used medicinally in the Pacific Islands. Tongan healers employed the thick woody stems of Faradaya amicorum as a bark infusion that was taken to relieve stomach ache – although the remedy was noted to have a purgative effect (Whistler 1992b). In Papua New Guinea, at Finschhafen (east of Lae on the Huon Peninsula) the stem sap of Faradaya parviflora was recommended for the relief of troublesome coughs – in combination with the administration of a soup made from Cassava or Tapioca (Abelmoschus manihot) (Woodley 1991; Holdsworth & Mahana 1983).
Fish Poison Wattles
A number of Australian Acacia have provided useful fish poisons due to their tannin content. Those with a piscicidal reputation included Hickory or Blackwood(Acacia penninervis), Hickory (A. falcata), the Goobang or Native Willow (A. salicina var. varians), Silver Wattle (A. holosericea), Black Wattle (A. auriculiformis) and the Long Leaf Wattle (A. longifolia). Their deployment was a fairly easy undertaking, with the bark simply thrown into a stream or waterhole. Joseph Maiden commented on the efficacy of this strategy: ‘In the case of streams, stakes were placed across, and a few wisps of wattle bark thrown into the water. In a little while the fish seemed to be intoxicated, knocked against the stakes, appeared bewildered, and the blacks, posting themselves near the stakes, took them out
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of the water. This stupidity or intoxication only lasted for about an hour. The fish caught by this method are in no way impaired as an article of food’ (Maiden 1894).
Acacia penninervis. The use of Hickory or Blackwood illustrates how simple fish poisoning strategies could be: ‘The bark (and according to some, the leaves) of this tree [Acacia penninervis] was formerly used by the aboriginals of southern New South Wales for catching fish. They would throw the bark or leaves into a waterhole, when the fish would rise to the top and be easily caught. Neither the leaves or the bark contain strictly poisonous substances, but like other species of Acacia, they would be deleterious owing to their astringency’ (Maiden 1888). (Image courtesy: Donald Hobern, CSIRO)
The explorer Thomas Mitchell, on 28 October 1846, illustrated the native wattle and provided an eloquent early description of it. In front of his tent there ‘grew a picturesque tree: the half-dead, half-alive aspect presented by the same sort of tree, was not unfrequent in the Australian woods; and I was induced to sketch this specimen, as highly characteristic of the scenery. These trees, “so wither’d and so wild in their attire,” generally appear under the shelter of other taller trees; have half their branches dead, the part still in foliage drooping like the willow, the leaf being very small. It is an Acacia (A. varians), and I was informed by Yuranigh that it is the Upas5 of Australia; the natives call it “Goobang,” and use a bough of it to poison the fish in waterholes. They are too honest and fair in their fights to think of poisoning their weapons. The aspect of this halfdead tree is certainly characteristic of its deleterious qualities, in the wild romantic outline resembling Shakespeare’s lean, poison-selling apothecary.’ 5 Upas was a well-known poison used for hunting purposes in Asia. It was sourced from the Upas tree (Antiaris toxicaria) or from various species of Strychnos.
In other areas different methods were employed. Fred S Brockmann, in A Report on the Exploration of North-West Kimberley (Western Australia) mentioned a somewhat more complex method of using the toxin: ‘With the coarse grass and wattle-bark they make what looks like an enormous straw bottle; the inside of this they fill with the bark obtained from the root of a shrub [Acacia sp.] which grows along the banks of the rivers … and then drag it themselves near backwards and forwards through the pool, the result being that the fish become stupefied and come to the surface and they are easily caught’ (cited in Hamlyn-Harris & Smith 1916). Medicinally, Acacia was a very familiar antidiarrhoeal agent, as bark extracts had an astringent character due to their tannin component. They also had useful antiseptic wound-healing attributes. However, strong tannin solutions can easily disrupt gastrointestinal function, which can sometimes result in severe distress. Later studies also discovered other components with toxic potential (including saponins) that tended to caution against the indiscriminate therapeutic use of some species. The South Australian Lake Eyre Exploratory Expedition of 1874–75 recorded the following illustrative experiment at Kallakoopah Creek: ‘During the night I suffered very much from the effects of the water from Tommy’s Well:
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the Silver Wattle sticks which we put in it imparted a very disagreeable taste to the water and also rendered it a violent purgative and emetic’ (Cleland 1931).
Wattle ‘Curls’
Acacia mangium.
Developing fruit Acacia holosericea.
of
Wattles often provided a useful antiseptic wash, although some species had rritant potential: ‘I have seen many cases of so-called “sandy blight” of the eyes of bush people at times when there was no sand and no wind, and in people where every suspicion of a specific infection was excluded. In one case it was easy for me to trace the real cause. The bushman, who suffered from a very acute conjunctivitis, with swelling of the lids, had the fingers of both hands covered with a sticky substance, which, on being washed away in a small basin, caused a very marked frothing in the water. The “sandy blight” for the woodcutter was caused by the juice of “wattle curls”, brought in contact with the eyes by wiping them with the hand’ (Lauterer 1897). In 1897 Joseph Lauterer outlined the investigations that these early experiences inspired: ‘Dr TL Bancroft in a scrub on the Gregory River, by accidentally biting the pods of Acacia delibrata, found that it has a very disagreeable, acrid taste. It seemed so strange that an Acacia should have any but an astringent taste that a quantity of the pods were gathered with a view to ascertain if they contained a physiologically active substance. The result of Dr Bancroft’s investigation was the discovery of saponin in the pods of Acacia delibrata.’
While saponins demonstrate experimental toxicity, poisoning from these chemicals does not usually result from their ingestion due to inactivation in the gastrointestinal tract. However, their administration by injection was far more dangerous: ‘injected directly into the circulation they produce haemolysis, diuresis … and direct actions, especially on the central nervous system, which may be rapidly fatal. At first there are violent convulsions; then paralysis, especially of the respiratory centre’ (Sollmann 1949). In addition, toxic alkaloids were eventually identified in the stembark of a number of species – Acacia holosericea, A. polystachya (syn. A. leptocarpa) and A. maidenii. Wattle pods readily attracted the interest of the early Australian chemists, as African and Asian members of the genus were already familiar to them. Investigations by Joseph Lauterer noted their soapy potential: ‘A watery infusion of the “wattle curls” froths and forms a lather, when agitated, like a solution of soap, this property is due to the saponin, which has been obtained pure by me from the pods. The tannin has to be removed first from the inspissated infusion
Acacia cunninghamii, from Illustrations of the Botany of Captain Cook’s Voyage Round the World 1768–1717 (1902) by the Right Honourable Sir Joseph Banks and Dr Daniel Solander, James Britten, 1900–1905.
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or watery extract by shaking with ether, which does not dissolve the saponin … it is a white powder … I found 3% of saponin in the unripe pods of Acacia cunninghamii.’ This led to some extremely interesting findings: ‘it is beyond any doubt that our Brisbane “black wattle”, Acacia cunninghamii – although quite innocent when it blossoms and after it has borne fruit – contains a large amount of saponin in the unripe pods, and a small amount of it even in the leaves and in all green parts of the plant.’ A keen observer, Lauterer took an interest in the seasonal chemical changes that occurred in Wattle trees. Of Acacia cunninghamii and A. penninervis he wrote: These Brisbane ‘black wattles’ blossom in the month of September and show the pretty flowers for about a fortnight, after fertilization has taken place the pods begin to grow. In about 3 weeks they attain the length of 2 inches, with a narrow width and twisted appearance which has gained them the name of ‘wattle curls’ from the school children in the bush. In this state the pods have a purely astringent taste. They contain about 20% of catechutannic acid, and not a trace of saponin. They continue to grow during the fourth week. The tannin then disappears gradually, whereas saponin by degrees takes its place. The astringent taste gives way to an extremely nauseous, acrid, and disagreeable sensation on the tongue, especially on the back parts and the sides of it. This taste creeps over the whole tongue, if even only the tip of it is brought into contact with the bruised pod. If the juice of the pod is allowed to reach the back part of the tongue, it seems to irritate some branches of the nervus vagus, as it produces a short hacking cough, and the same
sensation as when the inside of the ear or the skin behind the ear is scratched with a sharp instrument (Lauterer 1897).
Fish Poisons for Treating Cyanobacterial Contaminants
(Above and below) Acacia colei var. colei.) Courtesy BR Maslin, WA Herbarium)
Acacia colei var. ileocarpa, pods and seeds. The use of Acacia colei and A. holosericea as fish poisons involved placing the crushed bark and leaves in a dilly bag (string bag), which was then soaked in a waterhole. (Image courtesy: MW McDonald)
The deployment of some fish poison plants may have had an unexpected benefit in terms of water purification. The problem of cyanobacterial contamination of water supplies results from the occurrence of ‘algal blooms’ (see Chapter 11). In many parts of the country these outbreaks have been the result of haphazard clearing operations, misuse of water resources, and decades of poor land management strategies. The deployment of fish poisons often meant that a waterhole could not be considered safe until the next rains came, thus it was unwise to use them without good reason. Certainly a waterhole with a scummy algal bloom would not make an appealing water resource – and may well have made such waterholes ready candidates for the use of fish poison plants. The use of Acacia, as well as Duboisia hopwoodii, for this purpose suggests a potential toxic effect on cyanobacteria. However, the tannins, alkaloids and saponins in Acacia colei probably degraded fairly quickly, although the activity of Duboisia hopwoodii was likely to be quite different due to its alkaloid components (anabasine, nicotine, nornicotine). Interestingly
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nornicotine degraded into a non-toxic alkaloid form (myosmine) within a month (possibly earlier), although the residual potential of the other alkaloids remains unknown. Investigations of the toxic activity of extracts from Acacia colei and Duboisia hopwoodii on cyanobacteria have given variable results, which has left their hazardous potential as residual poisons open to debate. Microcystis aeruginosa was inhibited (not destroyed). A greater level of activity was shown against Anabaena circinalis and Nodularia spumigena. It is interesting that variations in the practical activity of the piscicide are likely to have been influenced by material selection and dose. Studies of Duboisia hopwoodii leaves have shown that alkaloid activity was reduced by over two-thirds during the drying process. Traditional methods of application, utilising fresh plant materials, could well exhibit different outcomes against cyanobacteria (Sadgrove 2009).
Toxic Puzzles: Native Stock Poisons
Stock poisoning has been a significant obstacle for Australian graziers since the very first runs were established across the country. A great deal of the knowledge of the toxic effects of fodder vegetation came from episodes of poisoning involving plants that were grazed along the stock routes. Selwyn Everist, in his presidential address to the Royal Society of Queensland in 1962, highlighted the persistent nature of the problem: It is difficult to assess the monetary value of losses due to poisonous plants, but even today it is by no means inconsiderable. One would expect that losses due to plant poisoning would decline as methods of animal husbandry become more intensive and our knowledge of toxic plants increases. To some extent this has happened, but the danger of plant poisoning still exists. For example, last year more than a thousand sheep in one flock died within six hours of their return to their home property, and in another instance more than a hundred cattle died when travelling a well-used stock-route in south-western Queensland. In each case the toxic plant responsible was well known and the mortalities could have been avoided. The losses were due to ignorance or carelessness on the part of those responsible for looking after the animals. Toxic plants are still with us and in most cases it is impractical, impossible or even undesirable to eradicate them (Everist 1964)
His words could be equally true today. In the field, different species of Acacia can be hard to identify clearly. The resultant difficulty in species differentiation can easily lead to confusion between toxic and non-toxic species. For example, Acacia crassa, A. concurrens, A. longispicata and A. leiocalyx have all been misidentified as the toxic A. cunninghamii. The non-toxic Gidyea, Acacia cambagei, was similar in appearance to the highly poisonous Georgina Gidyea or Gidgee (Acacia georginae) – and the leaves and flowers of both species had a ‘characteristic odour resembling that of rotting onions, particularly when the air is damp.’ Although the seeds and pods differed, this could be used for identification purposes only when the plant was fruiting (Everist 1981b). Obviously, such mistakes could have important ramifications. A number of other Acacia were suspected poisons, but definitive evidence was difficult to establish, as Selwyn Everist commented: ‘Several other species of Acacia have been found to contain potentially toxic substances but either no record of good field evidence is available to indicate that they are poisonous, or their toxicity is not proven by feeding tests’. This included the Black Sally Wattle or Black Wattle (Acacia salicina) in Queensland. A further complication could be linked to seasonal forms of toxicity. For example, although usually regarded as a good fodder plant, the leaf of the Currawang (Acacia sparsiflora) was suspected of poisoning sheep during drought. Cyanogenic toxic principles were isolated from a number of other Acacia species, including the Coast Myall or Sally Wattle (A. glaucescens), A. burrowii, A. cheelii, the Sydney Golden Wattle (A. longifolia), and the Ram’s Horn tree (A. oswaldii). (Everist 1981b)
Hordenline and Hallucinogens
Acacia holosericea was a fast-acting piscicide that was effective within half an hour of its use. The bark contains around 4 per cent tannin, and the saponin-rich green pods have been used as a bush soap due to their frothing qualities. Acacia holosericea is of further interest because it contains an alkaloid, hordenine (N,N-dimethyltyramine 1.2%), that has been used as a heart muscle stimulant– although, in small doses, it can have intestinal muscle relaxant effects (Hiddins 1999; Lassak & McCarthy 1992; Barr 1988). The compound also has
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known as Foxtail Lilies or Desert Candles, are native to the high plains regions of central and western Asia. Hordenine has another couple of unusual sources – southern African succulents known as Carrion flowers (for their aroma) and Starfish flowers (for their appearance) from the Stapelia genus. Red marine algae (e.g. Mastocarpus stellatus), which have been used as a source of carrageen, were another unexpected hordenine resource. Acacia holosericea.
diuretic, antibacterial and antibiotic properties that may have influenced the medicinal use of some plants. Certainly, the disinfectant attributes of hordenine could be useful for treating dysentery. However, while the compound is generally regarded as having low toxicity large doses can have a hypertensive effect due to an ephedrine-like action (Southon 1989). Hordenine, which was originally isolated from sprouted Barley (Hordeum vulgare), is present in diverse plants with quite different family affiliations. They include grasses, cacti and lilies (Southon 1989). Hordenine is prevalent in the Amaryllidaceae – for example, in the Crimean Snowdrop (Galanthus plicatus subsp. byzantinus) and the Eremurus genus (E. fuscus, E. luteus, E. regelli and Eremus transchanica). The latter,
Hordeum vulgare, Barley. (Courtesy: Lucas Hirschegger, Wikipedia)
Carrion flower, Stapelia gigantea. (Courtesy: Michael Joachim Lucke, GFDL)
There are other chemical links of interest between hordenine-containing plants. Hordenine is present in fairly high amounts in a number of cacti, some of which have hallucinogenic properties – they include the Peyote (Lophophora williamsii), San Pedro Cactus (Trichocereus pachanoi) and the Peruvian Torch Cactus (T. peruvianus). Mescaline (3,4,5-trimethoxyphenethylamine) is the main hallucinogenic alkaloid present in these species. There are some members of the Fabaceae (legumes) that also contain this hallucinogen – among them the Berlandier Acacia (Acacia berlandieri) from southwest USA. This species, which has a complex chemistry, contains additional hallucinogens (including DMT: dimethyltryptamine), various alkaloids and trace amounts of amphetamines. Similar chemical components have been found in Acacia rigidula, which comes from the same region. The Taiwan Acacia (Acacia confusa) also contains tryptaminederived hallucinogenic components. DMT has been found in a few Australian Acacia species, albeit in low amounts (around 0.25–0.35%):
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Lophophora williamsii. (Courtesy Peter Mansfield, Wikipedia)
A. maidenii and A. phlebophylla, in addition to N-methyl tryptamine in A. maidenii (see: shamanaustralis.com.au for further details). The story of the investigation of some poisonous plants became a complex affair. One of the more infamous stock poisons was found to contain fluorinebased compounds, implicating some species of the Leguminosae. Cattle poisoning was once a common, albeit somewhat unpredictable, occurrence. Around the Georgina River basin in northwest Queensland, as well as in adjacent areas of the Northern Territory, such incidents were particularly likely to occur during the dry season or during periods of drought. Selwyn Everist noted: much of the ‘poison’ country is fairly well-grassed and has good supplies of drinking water for livestock. Ever since the region was first stocked late in the 19th Century, there have been sudden deaths of sheep and cattle, often associated with particular tracts of country watered by particular bores or waterholes. There is marked seasonal incidence, mortalities occurring mostly from October to December when grass is scarce and dry and animals obliged to travel long distances for water. As well as direct losses due to sudden deaths of animals, potential production is greatly reduced because of the risks involved in stocking particular areas. These risks are often not apparent until expense has been incurred in sinking bores that yield good stock water (Everist 1981b).
Investigations ultimately determined that the Georgina Gidyea or Gidgee (Acacia georginae), as well as a number of Gastrolobium and Oyxlobium species, contained fluoroacetate. There can be vast differences in the toxicology of the different species and of the
different parts of a plant. With regard to Gastrolobium, Selwyn Everist provides the following summary: ‘Some species are more poisonous than others. In all cases, flowers and seeds are most toxic; the leaves of some species are palatable and very poisonous, others are reputed to be unpalatable the less toxic. In some species young growth is reported to contain more toxin than older growth … The seedlings of some species are toxic, in others they are reputed to be harmless … In some species toxicity is not lost on drying, others are reported to lose their poisonous properties rapidly after cutting; seeds of all species retain their toxicity for a long time.’ Some can even be devoid of poisonous effects, ‘an observation that gave some support to the long-held belief of many graziers in the Northern Territory and Queensland that individual trees vary in toxicity and there might be “poison” and “safe” areas or watering points on the same property’ (Everist 1981b). Overall, Gidgee seeds were found to contain the highest concentration of toxin, with lower levels present in the pods, and even less in the leaves. The fresh shoots contained moderate amounts, more than the mature leaves. In general, it was recommended that cattle be kept away from fruiting trees. The consequences of poisoning were worse if cattle were being driven to another site, or if they drank water during the trip. These observations explained some of the discrepancies between various incidents and suggested a few solutions to the problem: ‘It is possible to run cattle on country where it [Gidgee] grows providing they are not subject to undue stress and are
Acacia georginae. (Courtesy Matthew Turner, flickr)
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removed to “safe” country during dry spring and early summer months when it is in fruit. It is of interest to note that stress induced by driving sheep too fast was suspected as a cause of stock losses by the early settlers in Western Australia’ (Everist 1981b). Obviously, determining the circumstances responsible for this type of poisoning was a very confusing task – for both grazier and scientist. A similar puzzling situation had been encountered previously with some other native plants. Even though it had been known since the early 1900s that species of Myoporum and Eremophila (notably E. maculata) caused intoxication in sheep and cattle, under some circumstances these shrubs could be safely used for fodder. Animals at risk were those who were unaccustomed to these plants in their diet or had been under stress. Animals grazing quietly in a paddock suffered no problems. Unsurprisingly, this led some to wrongly conclude that the plants were harmless (Dowling & McKenzie 1993; Everist 1981b).
Fluoroacetic Acid
Monofluoacetic acid was a difficult toxin to identify. It is colourless, tasteless, water-soluble and highly stable – which meant that plants containing it gave no indication of their potential toxicity. Indeed, it was not identified as being a naturally occurring substance until 1943, and one which, fortunately, is quite rare (Everist 1981a). Fluoroacetic acid is converted to fluorocitrate in the body – a compound with enzyme-inhibitory properties that allows the accumulation of citric acid in the tissues. Toxic levels vary for different animals: 0.25–0.5 mg/kg sheep, goats, cats, pigs; 0.5–1.25mg/kg horses; 47mg/kg man; 10–30mg/ kg fowls. While some native mammals and birds were reported to eat toxic plants without ill effect, a dog or cat eating the viscera of these animals would probably die (Everist 1981b). ‘The variability of the effects of the toxin was a further case of perplexity to the colonists because certain of the symptoms of poisoning resembled those of better-understood stock diseases. In addition, not all domestic animals were equally affected and the apparent immunity of the native fauna was
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Sign warning of the presence of 1080 poison (sodium fluoroacetate), near Lake Kaniere on the West Coast of New Zealand. This toxin has been used as baits for feral animals, although its safety has been questioned – at low temperatures, it decomposes very slowly in soil and water, resulting in its persistence in the environment. It is considered an inhumane form of poisoning by the RSPCA. (Image courtesy: Greg O’Beirne, Wikipedia)
possibly the most puzzing feature’ (Everist 1981a). The story of the discovery of the toxicity of the native monofluoacetic acid plants involved some rather tricky chemical and feeding investigations. In the late 1830s an enormous public debate centred around the conflicting opinions of two influential botanical experts, James Drummond and Joseph Harris. The fact that Gastrolobium and Oxylobium belonged to the Fabaceae family led these genera to be ignored for some time as poisonous plant candidates – this family contains numerous legumes that were generally considered to be nutritious fodder plants the world over. The unexpected variability in the toxicity of the native species was an obstacle of paramount importance to the study of these stock poisons. Even Drummond, who was aware of the poisonous qualities of the genus, consistently refused to accept that the York Road Poison (Gastrolobium calycinum) was toxic, ‘for he had observed pigeons feed on the seeds of the plant with immunity’. He knew the pigeon flesh had been eaten by men, although if dogs ate the discarded bones they could die in sudden agony (Everist 1981a). The explanation lay with later discoveries
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regarding how native animals metabolised the toxin – and some even acquired a level of tolerance from exposure to fluoroacetic acid. Where animals such as the Grey Kangaroo (Macropus fuliginosus), Bush Rat (Rattus fuscipes) and Brushtailed Possum (Trichosurus vulpecula) regularly encountered plants containing the toxin they developed enhanced detoxification capabilities. Indeed, native marsupials were found to deploy an unusual biochemical method of detoxification, which does not occur via gut processes as one would normally expect. They actually absorb the toxin into their tissues where it is rendered harmless. Bronze-wing pigeons (genus Phaps) employ this type of protective mechanism. Toxins have been found in the birds’ bones, but not the flesh, which suggests that it is sequestered into bone or bone marrow (Everist 1981b).
Gastrolobium bilobum. (Courtesy: Graham Prichard, flickr)
Oxylobium Wikipedia)
ellipticum.
(Courtesy:
Melburnian,
Selwyn Everist notes: ‘In hindsight it is easy to imagine the anxiety and uncertainty of the colonists. The experts on whom they relied were searching for a substance which they had no means of identifying except by empirical means. The fact that the experts … held divergent views only added to the confusion surrounding the deaths of stock.’ Drummond commented: ‘it is very difficult to analyse unknown vegetable poisons or to explain their effect on animal life’ – a sentiment with which Everist concurred: ‘The truth of this remark is evidenced by the fact that it was not until more than 120 years later that the toxin (monofluoroacetic acid) in these particular poisonous plants was identified’ (Everist 1981a). Twenty-seven species of Gastrolobium and seven species of Oxylobium were eventually found to contain fluoroacetic acid as their toxic principle. A number of Western Australian species are among the most toxic of these plants. They include the widespread Desert Poison Bush (Gastrolobium grandiflorum), which ranges from Western and Central Australia to Queensland. Other common toxic species are very aptly named: Heart-leaf Poison (Gastrolobium bilobum), York Road Poison (G. calycinum), Rock Poison (G. callistachys), Wodji Poison (G. floribundum), River Poison (G. forrestii), and Champion Bay Poison (G. oxyloboides) (Everist 1981b).
Dichapetalum cymosum (Dichapetalaceae family). Sodium fluoroacetate was first identified in this Southern African shrub by Marais in 1944. (Image courtesy: Prof Christo Botha, University of Pretoria)
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Unique Selenium-accumulation Plants
Melilot (Melilotus indica).
The Australian shrub Mapoon (Morinda reticulata).
Melilot (Melilotus indica) is a common pasture plant, native to the northern hemisphere and naturalised in Australia, that hyperaccumulates selenium. Mapoon (Morinda reticulata) is a small Australian shrub with a limited distribution in northern Queensland on the Cape York Peninsula, extending no further south than Cooktown, that exhibits the same
characteristic. While it has been responsible for stock poisoning, only horses developed abnormalities (hair loss from the mane and tail, abnormalities in the hooves with resultant lameness) while cattle grazing the same land were unaffected. Mapoon is known to hyperaccumulate selenium even in soils that contain minute amounts of this mineral. It appears that despite a paucity of this element in surface soils the plant actively sources the mineral from deeper soil levels where the underlying rock naturally releases it into the earth. The leaf concentrations of selenium could be highly variable: ranging from 1.5 ppm (in an old fibrous sample) to 1,141.0 ppm (young leaves). Cases of poisoning were more likely to occur during spring and early summer, when the horses favoured the succulent new shoots that sprout after land clearing (Everist 1981b). This herb is of interest medicinally because of a note regarding its use as a contraceptive. Aboriginal women in the Cooktown area were reported to have taken a decoction of the leaf and root – which does not appear to be associated with selenium poisoning (Webb 1969). There is no indication as to the effectiveness of the treatment and little comment can be made regarding its validity or the compounds responsible. Selenium Weed, Neptunia amplex-icaulis, is another selenium-concentrating native that has been responsible for livestock poisoning in Australia. This is usually associated with a prolific growth habit that can occur on soils containing high levels of selenium. Selenium concentrations in the plant can vary enormously – ranging from 25.7 mg/kg to 4,434 mg/kg (average 1023 mg/kg). Fortunately it tends to grow fairly sparsely and is generally avoided by stock (Dowling & McKenzie 1993).
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
Medicinal Albizia Albizia in Austral
Various Australian species of the genus Albizia (family Mimosaceae) have been utilised medicinally. The genus previously contained numerous Australian representatives but, over time, classification changes have occurred. Albizia canescens, A. carrii, A. procera and A. retusa are the only native species that remain in this genus, along with a couple of rare Albizia species: ‘Windsor Tableland’ and ‘South Percy Island,’ which are found in northern Queensland. A. lebbeck also deserves mention as it is naturalised in the Northern Territory, Western Australia and Queensland. The reclassified species were placed in Archidendropsis, Archidendron, Paraserianthes, Samanea and Vachellia: • Archidendropsis: Albizia basaltica is now Archidendropsis basaltica; A thozetiana is now Archidendropsis thozetiana; A. xanthoxylon is now Archidendropsis xanthoxylon) • Archidendron: Albizia hendersonii is now Archidendron hendersonii; A. lucyi is now Archidendron lucyi; A. muelleriana is now Archidendron mullerianum; A. ramiflora is now Archidendron ramiflorum; A. tozeri is now Archidendron grandiflorum; A. vaillantii is now Archidendron vaillantii. • Paraserianthes: Albizia lophantha is now Paraserianthes lophantha; A. toona is now Paraserianthes toona. • Samanea: Albizia saman is now Samanea saman. • Vachellia: Albizia sutherlandii is now Vachellia sutherlandii. Walter Roth (1903) elaborated on the custom of love charms, with reference to the Pennefather River, northern Queensland: ‘When a man fancies a woman, and he wishes to inflame her passions, he puts a stripe of red clay all the way down his flanks and along the outer sides of his lower limbs, while at the same time he smears over the front of his body a preparation (kotenui) made from the inner bark of the tchannan (Denhamia obscura,
The Pink Laceflower, Archidendron grandiflorum, is an attractive native rainforest tree found in the northern Queensland and Cape York, as well as northern New South Wales and southern Queensland. It also ranges overseas to Papua New Guinea. Interestingly, it was one of the few plants noted to have been utilised as an aphrodisiac by Aboriginal people (Cribb & Cribb 1981).
Meisn.), or tre-inni (Pithecellobium grandiflorum, Benth.) mixed with charcoal, which gives him a peculiar scent. He then passes close to her; she both sees and smells him, and gets her passions excited.’ The genus Albizia is widespread, being found in Asia, Africa and Australia.6 It contains a number of saponin-containing plants that have been used for fish poisoning purposes around the world. In Asia Albizia saponaria and A. procera were utilised – although in Queensland, Aboriginal people regarded the latter as a less desirable alternative to other plants in common use. In Indonesian Borneo Albizia chinensis had a similar reputation, the fresh bark simply beaten in the 6 Older texts often spell the genus Albizzia.
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water to kill the fish further downstream. The fact that many of the genus contain appreciable amounts of saponin led to the popular use of a few species as soapsubstitutes. Indeed, Albizia saponaria once achieved commercial importance in eastern Malaysia.7 The bark was easily harvested, readily peeling off the tree when it was loosened with a mallet – although it had a disagreeable aroma that improved as it dried (Leaman 1991; Burkill 1935; Hamlyn-Harris & Smith 1916). The saponin containing-root (10% saponin) of Albizia amara was likewise suitable for washing purposes, as was that of A. lebbeck (Watt & BreyerBrandwijk 1962). Joseph Maiden mentioned that the root of a West Australian species, Albizia lophantha, contained about 10 per cent saponin. He commented that the ‘leaves bark, root and pods of all Australian species of Albizzia and Pithecelobium8 should not only be examined for saponin but also for Pithecolobine, an amorphous alkaloid, a deadly fish-poison, found in the bark of P. bigeminum and P. saman’ (Maiden 1898). Archidendron vaillantii (syn. Albizia vaillantii, Pithecellobium vaillantii) was a related saponincontaining species of toxicological interest that also contained alkaloids: ‘The pods contains beans which possess a black colour, and nauseous hot taste. The bark is also hot and acrid … The bark was found to be more poisonous than the bean or leaves … This substance kills by paralysing the reflex function of the spinal cord’ (Maiden 1889). A nasty toxin indeed – seeming to have the same CNS paralysing properties as pithecelobine. Even today little else is known about this rainforest plant. 7 Henry Burkill made an odd comment with regard to the use of this species: ‘It is a strange story that in Celebes the bark is kneaded with the tubers of Dioscorea hispida [a species with a very toxic reputation] when they are prepared for food ... because to add a poison to a poison when both have to be removed before the food is ready, is a process for which the reason must be peculiar’ (Burkill 1935). It would appear that the combination of the two toxic plants was thought to have a neutralising effect – although the processing procedure itself may well have facilitated removal or deactivation of the poisonous components. 8 Australian species that were formerly placed in the genus Pithecellobium (sometimes spelt Pithecolobium in the older literature, hence the chemical name pithecolobine) were later re-classified as Archidendron and Pararchidendron. Samanea saman and Cathormion umbellatum were also once classified as Pithecellobium. The synonym Albizzia [sic] has also been applied to some species. While Pithecellobium is no longer relevant to Australian native species, this classification continues to be a matter of substantial debate overseas – with species being variously assigned to Pitheceollobium, Albizia and Abarema. There are diverse other Fabaceae genera (Ingeae tribe), such as Inga and Zygia, to which the synonym Pithecellobium may have been applied at one time or other – particularly those from Central and South America.
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There are around 11 species in the attractive ornamental genus ArchJ273 J273idendron which were originally classified as Pithecellobium. The Salmon Bean, Archidendron vaillantii, is native to the rainforests of northern Queensland.
Anticancer Albizia
Investigations have indicated Albizia lebbeck (roots, stem bark) has anticancer potential (Kapoor 1990) – as have extracts of a number of other species in this genus. They include Albizia adianthifolia, A. procera, A. chinensis (saponins), A. coriaria, A. gummifera and A. schimperiana (Liu 2009; Note 2009; Cao 2007; Haddad 2004; Satyavati 1976). Albizia julibrissin extracts have attracted the most interest, notably the julibroside saponins (Hua 2009; Roy 2008; Zheng 2006a, 2006b; Zou 2006; Won 2006; Liang 2005; Jung 2003; Moon 1985). Antioxidant compounds (hyperoside, quercitrin) have also been isolated from foliage, flower and whole plant extracts of this species (Vaughn 2007). Hyperoside has anti-inflammatory and diuretic properties, while quercitrin has cellular repair potential for the gastrointestinal tract (Ekenseair 2006).
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The Siris Tree (Albizia lebbeck
Sawdust Irritants
Paraserianthes toona. The Siris tree naturally favours the edges of the rainforest near open woodlands. (Image on right courtesy: Kim and Forest Starr, Hawaii)
The Siris tree (Albizia lebbeck) is native to tropical Australia, ranging from Cape York to the Kimberley region of Western Australia, and to tropical southern Asia. The form commonly found in cultivation, however, was introduced at an early date, probably from imported Indian seed stock. The Siris tree has been widely planted as an ornamental shade tree and fodder resource. It has potential as a high-protein animal feed during dry seasons – the flowers, fruit and leaves are all edible. It also has environmental advantages related to soil and ground-water conservation, as well as benefiting the growth and quality of pasture grasses. The tree also yields a high-quality timber known in Europe as East Indian walnut (Lowry 1989, 1993). The Siris tree has been extensively deployed overseas as a medicine. The bark has been valued as an anti-inflammatory for conditions such as arthritis9, bronchitis, ophthalmia and gum inflammation – as well as being used to treat leprosy, paralysis and worm infestations. The whole plant was applied to snakebite and scorpion stings – as well as being utilised for treating bone fractures. Moreover, the leaves had an unusual reputation as a useful treatment for night blindness. The astringent effects of the seeds and bark saw them utilised for treating gastrointestinal disorders (diarrhoea, dysentery, haemorrhoids) and gonorrhoea. Powdered, the root-bark was also said to strengthen the gums (Babu 2009; Kapoor 1993; Satyavati 1976). 9 The flowers have also been utilised as an anti-arthritic remedy (Babu 2009).
Acacia Cedar or Red Siris (Paraserianthes toona, formerly Albizia toona) is a Queensland endemic species that is found from the Cape York Peninsula to coastal Central Queensland. It gained the alternative name of ‘Mackay Cedar’ due its harvesting for timber around this town; unfortunately, it can present an occupational hazard for sawmill employees. Red Siris has been responsible for epistaxis (nose bleed) in workers cutting and dressing the timber. Albizia lebbeck sawdust is also liable to induce sneezing attacks (Webb 1948; Burkill 1935). Albizia anthelmintica appears to have similar allergic potential (Khalid 1996) – as does Falcata wood (A. falcataria), which has been linked to the development of work-related asthma (Tomioka 2006).
Falcataria moluccana. (Images courtesy: Kim and Forest Starr, Hawaii)
The Moluccan Albizia (Falcataria moluccana, formerly Albizia falcataria or Paraserianthes falca-
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taria) is a fast-growing Southeast Asian timber tree, whose distribution ranges to New Guinea. It has been widely used in Malaysia and Indonesia as a shade tree for plantation crops. The tree yields an extremely useful soft timber that is suitable for making matches, chopsticks, packing cases, pallets and paper products, but it can quickly become a weedy pest given the right conditions.
Albizia procera
Albizia procera (Courtesy: JM Wikipedia)
pods. Garg,
The White Siris, Albizia procera10, has a similar distribution to the Acacia Cedar (Paraserianthes toona) in Queensland, although A. procera extends to the Northern Territory and Western Australia – as well as being found overseas in Malesia and Asia. The inner bark was utilised at Proserpine (on the central Queensland coast) as an Aboriginal fish poison and, although studies did not confirm its efficacy, its potency could be seasonal in nature (Webb 1948; Hamlyn-Harris & Smith 1916). The pods have been utilised medicinally as a local application for treating ulcers, while the leaf has been utilised as an insecticide. Various Albizia procera extracts have shown hypoglycaemic (pods, stem bark) 10 The name White Siris can also be applied to Ailanthus integrifolia and A. triphysa, which belong to a different family – the Simaroubaceae.
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and anticancer (root, pods) activity. The pods also had antiprotozoal activity against the parasite Entamoeba histolytica (Satyavati 1976). Albizia lebbeck bark contains a diversity of compounds of pharmacological import, including tannin (polyphenols such as epicatechin), saponins (albiziasaponins) and triterpenoids (lupeol, stigmastadienone). Stem-bark extracts have good antimicrobial properties – that is, antibacterial and anti-candidal11 – and anti-trichomonal activity. It has been efficacious as a remedy for treating Candida infections. Various extracts (leaf and bark) have demonstrated anti-inflammatory, analgesic, antiulcer and cholesterol-lowering activity, as well as a supportive effect on adrenal function. Traditionally, the herb has been used for conditions that impact on the immune system such as bronchial asthma and eczema, and reactions caused by insect bites. Indian studies of the anti-allergic (anti-anaphylactic) effects of Albizia lebbeck have shown significant immunomodulating benefits via an inhibition of the early processes of sensitisation, as well as beneficial effects on antibody production and stabilisation of normal cellular function. Catechin has been identified as one of the main anti-allergic components of the herb (Venkatesh 2010; Babu 2009; Saha & Ahmed 2009; Shashidhara 2008; Besra 2002; Barua 2000; Bone 1999; Kapoor 1993; Ganguli & Bhatt 1993). Clinical studies of Albizia lebbeck for treating asthma have shown that conditions of recent origin (within two years) tended to have an excellent response to treatment. However, in chronic states the results were more unpredictable, with some individuals deriving benefit while others did not. This was because the herb’s activity was not linked with antispasmodic or anti-histaminic activity but was attributed to an anti-allergic effect. The remedy would therefore be more appropriate for asthma that was of 11 In addition, the African species Albizia anthelmintica and A. gummifera have shown good anti-candida activity, with the latter possessing antibacterial activity against Streptococcus pyogenes and S. pneumoniae (Mbosso 2010; Unasho 2009; Runyoro 2006). A Thai medicinal herb, Albizia myriophylla, has also shown significant anti-candidal activity that is of clinical interest (Rukayadi 2008). The latter contains a range of saponins, one of which (albiziasaponin B2) had intensely sweet attributes – being 600 times more potent than sucrose (Yoshikawa 2002).
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allergic origins. External applications for skin disorders such as weeping eczema likewise gave extremely good clinical results. The fact that the herb had a suppressive effect on hypersensitivity responses has suggested that it could also have good potential for treating hayfever (allergic rhinitis)12 (Bone 1999; Tripathi 1979a, 1979b). Additional research has suggested that the antioxidant potential of the herb could be useful for preventing liver and kidney tissue damage in diabetic individuals (Resmi 2006). 12 The herb has been incorporated into a combination product (Aller-7) used clinically for treating this condition. The other components are: Phyllanthus emblica, Terminalia chebula, Terminalia bellerica, Piper nigrum, Piper longum and Zingiber officinale. The remedy has shown potent antihistaminic, anti-inflammatory, antispasmodic, anti-oxidant, and mastcell stabilisation activities (Amit 2005, 2003; Pratibha 2004).
Medicinal Seed Pods
Albizia lebbeck pods and seeds. (Courtesy: Kim and Forest Starr, Hawaii)
Siris Tree seed extracts have shown good antidiarrhoeal activity that supports its traditional use for treating this condition (Besra 2002). Interestingly, recent studies have isolated a haemolytic protein (lebbeckalysin) from seed extracts that has shown antifungal activity (against Rhizoctonia solani) and antibacterial
activity (against Escherichia coli), as well as antitumour potential (Lam & Ng 2011). Extracts of the pods (and isolated saponins) have shown antifertility properties (inhibition of sperm formation)13 in animal studies, without significant toxicity, with potential for the development of a male contraceptive (Gupta 2006, 2005, 2004). Interestingly, the flowers have been utilised in Indian traditions as a remedy for spermatorrhoea (Watt & Breyer-Brandwijk 1962). Many Albizia species have been used as antiinflammatory and healing remedies for numerous skin problems and infections (Vijayakumar & Pullaiah 1998; Patel 1986; Yeung 1985; Satyavati 1976; Watt & BreyerBrandwijk 1962; Quisumbing 1951; Burkill 1935): African traditions employed Albizia lebbeck for • wound healing and skin infections including ulceration, furuncles, and similar conditions; in China the powdered bark of A. julibrissin was utilised in the same manner. • Indian traditions employed leaf poultices of Albizia procera for treating ulcers – as was a paste of A. amara bark prepared with alcohol. The leaf of the latter was applied to erysipelas and abscesses, while the powdered seed (which is edible) had astringent properties.14 The seed oil has also been used in treatments for leprosy and leucoderma. • Indian traditions regarded Albizia lebbeck seed oil as being similarly useful for leprosy, and the seed paste for cervical gland enlargement and scrofulous swellings. A cataplasm of the flowers, which had emollient properties, was also useful for skin infections. • In Africa Albizia adianthifolia has been applied to scabies infections (from the mite Sarcoptes scabiei), which suggests the remedy had antiparasitic activity. A hot infusion of the bark and root was applied locally (Watt & Breyer-Brandwijk 1962; Quisumbing 1951). • In Papua New Guinea Albizia fulva was applied to cuts and sores to promote healing. The inner bark 13 Albizia chinensis, which has utilised as a spasmolytic and diuretic remedy, has also shown strong spermicidal properties (Rawa 1989). 14 Albizia amara fruit has been used as an emetic in Central Africa – as well as for treating coughs and malaria (Watt & Breyer-Brandwijk 1962).
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and sap were rubbed on the affected area daily and the bark then used as a bandage. In addition, a wash made from Albizia falcataria bark (scraped and squeezed in water) was useful for treating tropical ulcers (Holdsworth 1983; Holdsworth & Rali 1989).
A Chinese Sedative
Albizia julibrissin and A. kalkora have been officially used in traditional Chinese medicine as the sedative and tranquillising herb He Huan Pi.
Chinese medicine has highly valued Albizia as a tranquillising and sedative remedy. Albizia julibrissin flowers have long been utilised for treating insomnia, as well as being recommended for palpitations due to anxiety or other emotional upsets. The bark has similar sedative properties. The Reverend GA Stuart (1911) wrote eloquently of the remedy: It is considered to be an auspicious tree, promoting agreement and affection, and therefore is given a place among domestic shrubbery. Its leaves are also edible. The parts of plant appearing in the Customs Lists are the flowers, but the portions recommended to be used by the Pentsao are the bark and wood. On account of the auspicious character of this tree, its use in medicine is also thought to be attended with the happiest results: ‘promoting joy, assuaging sorrow, brightening the eye, and giving the desires of the heart’. In the treatment of disease, it is regarded as a tonic, vulnerary, sedative, anthelmintic, and as a discutient [a remedy that
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disperses morbid matter, e.g. swollen tissue, infections]. A gummy extract is prepared and used as a plaster for carbuncles, swellings, and as a retentive in fractures and sprains.
The bark has also been utilised for traumatic injuries, acting to promote blood circulation and relieve pain (Yeung 1985). There are some interesting investigations that support these traditional recommendations. Bark extracts have shown anti-inflammatory activity from a glycoside fraction, while flavonol glycosides (quercitrin, isoquercitrin) from flower extracts possess sedative properties (Qiao 2007; Kang 2000). Stem-bark extracts have shown anxiolytic and antidepressant activity (Jung 2005; Kim 2007; Kim 2004). The Brazilian Albizia inopinata has a similar central nervous system depressant (sedative) activity, as well as vasorelaxant hypotensive properties (Maciel 2004; Assis 2001; Pires 2000). In addition, Indian investigations have suggested that Albizia lebbeck has anxiolytic and nootropic effects, with benefits for brain and memory function in animal studies. Extracts have also demonstrated anticonvulsant activity (Chintawar 2002; Une 2001; Kasture 2000).
Antiparastic Albizia
Albizia anthelmintica. (Courtesy: Paul Latham, zimbabweflora.com.au)
The use of various species of Albizia as antiparasitic agents is supported by a number of investigations that show the genus has interesting potential for practical use, and as a source of compounds for drug development.
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Albizia anthelmintica. (Courtesy: Paul Latham, zimbabweflora.com.au)
Kenyan villagers have long employed Albizia anthelmintica as a worming agent in their sheep flocks. Studies have indicated the activity of the remedy ranges from good to excellent against a number of parasites including Ascaris lumbricoides, Haemonchus contortus, and Moniezia helminths. Some studies (but not all) have shown an effect equivalent, or superior to, conventional drugs. It is possible that variability in the preparation of extracts could account for differences in their activity (Grade 2008; Gathuma 2004; Githiori 2003; El Garhy & Mahmoud 2002). Some extracts were also highly effective against liver fluke (Fasciola gigantica) infection, with activity comparable to conventional treatment options (Koko 2000). The pharmacological evaluation of some additional species has been similarly inspired by their traditional medicinal use, notably as febrifuges for the treatment of malaria. They include herbs such as Albizia coriaria, A. gummifera, A. zygia and A. schimperiana, which have demonstrated strong antiprotozoal activity. The latter was said to be particularly useful as an antimalarial remedy, as well as for easing general discomfort and providing pain relief. It has also been utilised for bacterial infections (including pneumonia) and has demonstrated effective broad-spectrum antibacterial properties. Albizia versicolor is another antimalarial remedy with a similar antibacterial and antiparasitic reputation that was utilised in Kenya for treating venereal disease, cough and joint pain, and as a vermifuge for tapeworm. Alkaloids (spermine
alkaloids) were identified as active antiplasmodial components of Albizia adinocephala from Central America (Panama) and the African species A. gummifera, the latter being of particular interest for its synergistic effect with chloroquine as an antimalarial agent. Extracts also possessed good broad-spectrum antibacterial activity. Albizia chinensis has shown a selective activity against chloroquine-resistant Plasmodium falciparum. A few other species have antiparasitic potential against the disease vectors for conditions such as kala-azar, sleeping sickness and Chagas disease. Albizia coriaria demonstrated significant inhibitory activity against the leishmania parasite (Leishmania major), while A. zygia had antitrypanosomal activity against Trypanosoma cruzi (Kigondu 2009; Samoylenko 2009; Muregi 2007; Ndjakou Lenta 2007; Rukunga 2007; Geyid 2005; Rukunga & Waterman 2001). Bark extracts of Albizia anthelmintica however, were found inactive against the malaria parasite Plasmodium falciparum (Leanman 1995). Albizia lebbeck (stem-bark, root, seed-pod) extracts have also demonstrated interesting antiprotozoal, anthelmintic and molluscicidal activity that were attributed to their tannin and saponin components. Other species with molluscicidal properties include Albizia amara (seed), A. coriaria (bark) and A. zygia (leaves)15 (Kapoor 1990; Ayoub Hussein & Yakov 1986; Oliver-Bever 1986). Albizia zygia (syn. Acacia zygia) is an African species that yields a good quality timber. It also produces a highly viscous gum suitable for use as a stabiliser in food products such as ice-cream and as a thickening agent for pharmaceutical purposes (FemiOyewo 2004). (Image courtesy: Kim and Forest Starr, Hawaii)
15 A number of tannin-containing plants that were evaluated at the same time showed similar activity: Entada africana (leaves), Azadirachta indica (leaves) and Rosa gallica (petals) (Ayoub Hussein & Yakov 1986).
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Cassowary Pine
Albizia amara extracts have shown repellent effects against the mosquito vector (Aedes aegypti) for dengue fever (Murugan 2007). (Image courtesy: JM Garg, Wikipedia)
Deceptive Beauty: The Fish Poison Trees
The Barringtonia genus contains around 40 species. It has a fairly wide distribution, ranging from East Africa and Madagascar, to Taiwan, northeast India, Indonesia and Malaysia – as well as the Pacific Islands and Australia. Tropical Australia is home to four Barringtonia species – B. acutangula subsp. acutangula, B. asiatica, B. calyptrata and B. racemosa. The genus has a reputation as potent piscicidal agents which led to the common name ‘Fish Poison trees’. The use of the bark (sometimes the roots) of the Freshwater Mangrove (Barringtonia acutangula) is illustrative. The outer and inner bark were chipped off the tree trunk and beaten into small pieces, which were placed in a cylinder of paperbark. This was tied at each end, which made it easy to immerse and move around in the waterhole. The toxin was said to deplete the water of oxygen, which was later replaced by putting the leaves of the same tree into the waterhole16 (Lindsay 2001). The bark and fruit of Barringtonia racemosa was likewise regarded as a good piscicidal agent – as were the fruit and seeds of B. asiatica.
16 This suggests that the leaves were not considered to have toxic properties.
Cassowary Pine (Barringtonia calyptrata).
The Cassowary Pine (Barringtonia calyptrata) is a rainforest tree that favours a coastal habitat, often found near streams. It has a fairly wide range in northern Queensland, from Ingham to Cape York, and extends overseas to Papua New Guinea. The elegant drooping clusters of cream flowers are highly attractive to many insects. They are pollinated by the lovely Hawk Moths, and provide a nectar feast for blossom bats and many birds such as the rainforest honeyeaters and lorikeets. However, the Cassowary is possibly the only animal that finds the fruit palatable. The tree has a limited medicinal reputation with a leaf decoction (which contain saponins) being utilised by Aboriginal people for the treatment of chest pain (Lassak & McCarthy 1992; Webb 1960). The activity of these fish poison trees is based on their tannin and saponin content. However, their use had a serious drawback. The water remained toxic long after the fish were captured, which limited their use – and that of similar fish poisons. The unwise deployment of such piscicides could easily deplete fish populations and, in the long run, even prevent the natural restocking process. Their use was therefore accompanied by a reasonable amount of caution. Similar concerns have been associated with the use of these toxins overseas.
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Illustration of Barringtonia speciosa from Flora of the Philippines (Flora de Filipinas, Gran Edicion, Atlas II) 1880– 83 by Francisco Manuel Blanco (O.S.A.) The distinctive four-angled ‘box-fruit’ of the Beach Barringtonia (Barringtonia asiatica) can be found washed up along the tropical beaches of northern Australia and the Pacific Islands. They were once used as floats for fishing nets as underneath the leathery outer skin, they contain a spongy buoyant layer that covers the seed within. The fruit, which are designed to naturally stay afloat for long periods, can last up to two years in their marine travels.
A century ago Alvin Seale wrote of the use of Barringtonia speciosa (i.e. Barringtonia asiatica). In A Report of a Mission to Guam, Caroline Island (1901) he mentioned that problems had resulted from overfishing: In former times the natives caught and dried great quantities of fish by this means, a grand fiesta being held at certain seasons of the year. The Spanish authorities, however, finding that this was depleting the waters by killing young as well as old, abolished the method in 1894. When the Americans took possession the law was considered obsolete. By chance I was present at the first of these fiestas that had taken place for 7 years. Fully several hundred people took part in the fishing. An immense deep pool several hundred feet deep, a short distance inside the reef, was surrounded by a line of seines. At low tide about 1 barrel of this precious juice was poured into the pool. The effect was almost instantaneous; hundreds of fishes came gasping and struggling to the top of the water, where they were captured and killed by the natives. No ill-effects seemed to follow the eating of these poisoned fish.
Extracts were usually prepared from the crushed seed, although in some places the bark was also utilised.
The Beach Barringtonia (Barringtonia asiatica) is an impressive tree that ranges from the northern Australian rainforests to Southeast Asia – and from India to Madagascar. It has been used as a piscicide throughout much of the region and has numerous medicinal uses. It is a handsome feature of the tropical coast with striking filamentous blossoms that only open in the late evening. They produce a somewhat musty scent designed to attract pollinating moths. Discarded blossoms can be found littered on the ground the next morning – leaving an equally distinctive square-shaped fruit developing on the tree. In Hawaiian medicine a preparation of the flower, which has shown mild antifungal activity, was applied to burns and wounds (Locher 1995).
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Edible Cutnuts
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latter add support to these claims (Mathur 1983). In Fijian traditions Barringtonia edulis was utilised as a fish poison, although juice from the plant could have irritant effects on the eyes. In addition the leaves were ‘said to be a certain cure for erysipelas’, as well as being used to treat severe backache (Cambie 1986) – which suggests antibacterial and pain-killing attributes. Certainly preliminary studies of the analgesic potential of leaf extracts have suggested it deserved further investigation (Sampson 2000).
Myriad Medicinal Uses Barringtonia edulis is an extremely attractive small tree that is native to the Pacific Islands.
There are three edible species of Barringtonia known as Cutnut or Pilinut in the Pacific region: B. edulis, B. procera and B. novae-hiberniae. They share a very similar distribution, although Barringtonia procera is usually cultivated around villages and B. novae-hiberniae is a wild species. Barringtonia procera and B. edulis are found in the Solomon Islands, Vanuatu and Papua New Guinea – although B. edulis, which is not found in New Britain (PNG), extends its range to the Fijian Islands. Medicinal traditions have utilised the leaves of Barringtonia procera to treat ear inflammation and headaches. The bark sap has provided a remedy for ciguatera poisoning17, coughs, and urinary infections. A red-leafed form was also used as a contraceptive and abortifacient (Paku 2006). In Vanuatu an infusion of the inner bark was taken as a cough remedy, while toothache was treated with a mouthwash prepared from the chilled infusion (Bradacs 2011). The bark infusion has also been taken to induce abortion, as well as to induce sterility (Bourdy & Walter 1992). Interestingly, the Freshwater Mangrove (Barringtonia acutangula) was reputed to have similar properties (Perry & Metzger 1981). Studies that have shown anti-implantation activity for the 17 On Guam a stem-bark infusion of Barringtonia asiatica was also utilised for treating ciguatera poisoning (Bourdy 1992)
In Papua New Guinea the Beach Barringtonia (Barringtonia asiatica) was often employed as an antibacterial agent, with diverse interesting medicinal applications (Holdsworth 1986; Holdsworth & Corbett 1988): • The Beach Barringtonia has been widely utilised for treating skin problems. The juice of a fireheated leaf was squeezed onto the sores of yaws (an infectious tropical skin disease that causes ulceration of the extremities). On Manus Island the fruit was applied directly to sores. • The powdered nut infusion was taken to treat respiratory problems (cough, influenza, sore throat, bronchitis), as well as diarrhoea. • Scraped bark, combined with another unidentified plant and prepared as a concentrated infusion, was taken daily for tuberculosis. Betel nut (Areca catechu) and lime were chewed at the same time. • Powdered nut infusion was also said to be useful to counteract the development of splenic enlargement (splenomegaly) following malaria. • In Samoa the nut was likewise applied to wounds (dried or fresh), as well as being employed as a remedy for tuberculosis. The Freshwater Mangrove (Barringtonia acutangula) also gained a fairly extensive medicinal reputation throughout its range. Joseph Maiden noted: ‘In India an extract of juice obtained from leaves of this tree which, when mixed with oil, is used in native practice for eruptions of the skin18; kernels powdered and 18 Care needed to be taken with the fresh arid sap as it could ‘burn’ delicate eye membranes upon accidental eye contact, and skin exposure can result in dermatitis.
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• In Southeast Asia the sap was widely applied to stings and sores due to venomous insects. The subspecies Barringtonia acutangula subsp. spicata was also poulticed on ulcers and itchy skin problems. The root was regarded as having expectorant actions (Kapoor 1993).
Tropical Amoebic Dysentery
Despite its name, the River or Freshwater Mangrove (Barringtonia acutangula) is not restricted to a coastal mangrove habitat as it extends inland along streams and rivers. The tree also has a fairly wide range overseas, being found in Papua New Guinea and Southeast Asia, ranging to India and Afghanistan.
prepared with sago and butter are used in diarrhoea and mixed with milk they produce vomiting; the root is bitter and said to be similar to Cinchona, but also cooling and aperient [mild laxative]’ (Maiden 1889). It was regarded as being useful in treating feverish conditions such as malaria, and studies have shown extracts had hypothermic (temperature-lowering) properties (Satyavati 1976). In Southeast Asia its overall reputation was very diverse (Perry & Metzger 1980): • The fruit and the bark had astringent attributes, which led to the use of the latter as an antidiarrhoeal agent. • A wood infusion provided a useful haemostatic for treating excessive menstrual bleeding (menorrhagia). • In Southeast Asia the seed was used as a remedy for ophthalmia (eye inflammation). • The powdered fruit (roasted, powdered and mixed with sugar) was applied to the gums to treat gingivitis. • In the Philippines the bark was applied locally to heal wounds and the decoction taken as a stomachic. • Freshwater Mangrove has also been recommended for the treatment of respiratory disorders. The fruit was mixed with fresh ginger juice and taken for nasal catarrh, or it could be applied externally to the chest for pain relief. • A snuff of the powdered seeds was said to be useful as a headache treatment.
Cyst of Entamoeba histolytica.(Courtesy: US Centers for Disease Control (CDC), Public Health Image Library)
Barringtonia acutangula leaf juice has been widely taken as a bitter tonic and as a remedy for diarrhoea and dysentery in India and Southeast Asia (Kapoor 1990). Support for its use has been provided by studies showing that stembark extracts had antiprotozoal activity against Entamoeba histolytica (Satyavati 1976). This is the parasite responsible for tropical amoebic dysentery, which is characterised by a debilitating form of diarrhoea that can result in serious dehydration. Antiparasitic agents are the standard form of treatment. However, the condition can be compromised if the parasite penetrates the colon wall and causes ulceration. In some cases the amoeba can persist in the bloodstream to ultimately reach the liver (via the portal vein blood circulation), with the potential to cause abscesses and hepatic dysfunction, resulting in jaundice. Although relatively rare, the amoeba can infect other organ systems. In addition to the original symptoms of intestinal dysfunction, progressive systemic infection can therefore involve the lungs, brain, kidneys and skin. At this stage there is a high incidence of fatalities. Another unseen hazard involves individuals who do not develop
FOAMING FISH POISONS
symptoms at all. They become ‘carriers’ of the amoebic cysts, with the potential to act as a reservoir of infection for others. Emetine was formerly regarded as a specific treatment for amoebic dysentery. Although it does not cure the problem, it effectively controls the symptoms associated with the severe intestinal infection. The drug has been valuable for the treatment of amoebic hepatitis, as well as lung, brain and skin amoebiasis. The great drawback to its use is that it does not eradicate the cysts and is ineffective in symptomless carriers. Chloroquine (which is less toxic than emetine) is a treatment alternative useful for some cases of amoebic dysentery – although it is not effective where there is intestinal dysfunction, or in cyst carriers Today metronidazole (i.e. Flagyl) remains the mainstay of most therapies. This drug, which was discovered in the late 1950s, owes its origins to investigations of the antibiotic azomycin, which had been isolated from a species of Streptomyces. Unfortunately, metronidazole needs to be used with care as it can have a range of debilitating sideeffects – nausea, anorexia, diarrhoea, epigastric distress, abdominal cramping, headache, vomiting, dizziness and vertigo – as well as occasional nervous system dysfunction and fungal infections (e.g. moniliasis).
Emetine from the Merck Index of 1968.
The root of the South American shrub Ipecacu-anha (Psychotria ipecacuanha syn. Cephaelis ipecacuanha) was traditionally utilised in the treatment of dysentery, and from this source
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Ipecacuanha herb from Koehler’s Medicinal Plants, 1887.
the drug emetine was discovered in 1817. The main isoquinoline alkaloids found in the root are emetine and cephaeline (98% of root alkaloids) (WHO 2007). Dosage is important with the use of this drug. At around 15–30 grains the root was emetic, while a much smaller dose (1/4–2 grains) was traditionally utilised as an expectorant remedy. The latter suited it for use in respiratory disorders (bronchitis, asthma, whooping cough) to remove thick phlegm congestion. Very small doses were also said to stimulate the appetite and digestive functions (Grieve 1931). Ipecac root gained more fame as an emetic agent and was highly regarded as a poison antidote. It was once officially recognised in numerous pharmaceutical texts. Syrup of Ipecac, which contained around 24 mg emetine and 31 mg cephaeline per 30 ml, was a standard component of the household medicine cabinet. However, recent investigations have not supported its use as an emergency treatment in hospitals, as it may compromise the efficacy of other treatments, particularly activated charcoal, and can decrease the absorption of some drugs
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(e.g. paracetamol, tetracycline, aminophylline). It is important to realise that limits on the practical use of Ipecac are linked to considerations of dosage and the form of the drug. For instance, the standard tincture preparation is 14 times stronger than the syrup. Prolonged ingestion of excessive doses, not unexpectedly, can cause adverse reactions (particularly in the gastrointestinal tract) and it is not considered safe for individuals subject to cardiac problems, seizures or suffering shock. It is also contraindicated in poisoning due to corrosive substances, and its traditional use as abortifacient suggests it should not be used during pregnancy. In addition, the root powder has irritant effects on the skin, and on the respiratory tract if inhaled (WHO 2007).
Pulvis Ipecac from Phillips’ Translation of the Pharmacopoeia Londonensis, 1841
The third species of interest among the native Australian Barringtonia is B. racemosa, the saponincontaining seeds and bark of which have been in widespread use as a piscicide. The bark, which was cut into small pieces and hammered to a fine consistency on a stone, was left to infuse in water before being used as a fish poison by Aboriginal people in northern Queensland. It was a quick-acting drug as the fish were stupefied within 15 minutes (Roth 1901). This species has had an extensive medicinal reputation throughout Southeast Asia, Papua New Guinea and Australia. Triterpenoid saponins (barringtogenols) have been isolated from the fruit, seed and leaf of Barringtonia racemosa – as well as barringtonic and acutageic acids (Lassak & McCarthy 1992; Webb 1948).
Diverse other components in stem-bark extracts are of pharmacological interest: phenolics (gallic and ellagic acids), dihydromyticetin, sterols (stigmasterol), betulinic acid, lupeol, bartogenic acid (Sun 2006; Yang 2006). The tannin-rich root and stem bark have useful astringent properties. The antibacterial and antiviral actions of tannin would doubtless contribute to efficacy as a remedy for skin conditions, as well as for treating throat soreness and diarrhoeal disorders. In the Indochinese region (a floristic region in Southeast Asia)19 the bitter-tasting roots were used as a febrifuge and for treating measles, while fruit was taken for cough and asthma. The crushed kernels20 were mixed with flour and oil for use as an anti-diarrhoeal remedy, while the charcoaled (ashed and powdered) seed was incorporated into a remedy used to treat colic. In the Philippines, the heated fresh leaves were applied locally to treat stomach ache or rheumatic pain (Perry & Metzger 1980). In Ayurvedic medicine the fruit has also been utilised for the treatment of pain, inflammation and rheumatic conditions (Patil 2009). On the Malay Peninsula and Indonesia the use of Barringtonia racemosa in the treatment of skin disorders has been widespread. In Malaysia, poultices of the leaf, root and bark were applied to itchy skin problems – as well as chickenpox (pounded leaves) and measles eruptions (root infusion). A paste made from the grated bark was smeared over scabby sores in Indonesia. The juice from the fruit, which was used similarly, was noted to have anti-parasitic properties – while the bark and seeds had anthelmintic effects.21 A decoction of bark was also used as an antirheumatic lotion (Perry & Metzger 1980; Zakaria & Mohd 1994). The latter appears to be similar to the use of an Aboriginal preparation on the Bloomfield River in northern Queensland, in which the bark was hammered and dipped into boiling water before dabbing it over the body of a sick person. There is also a note that the remedy was used in ‘non-venereal stricture’ (stricture refers to a narrowing of the urethra, usually due to infection or inflammation, that results in difficulty urinating) (Roth 1903). 19 This region includes former French Indochina (Cambodia, Laos, Vietnam) and parts of mainland Southeast Asia (Myanmar, Singapore, Thailand) and, possibly, peninsular Malaya. 20 In light of the toxic reputation of the kernels, this seems to be an unusual recommendation. One can only assume that the processing undertaken had a detoxification effect. 21 The bark has also shown effective insecticidal activity against thrip and aphids.
FOAMING FISH POISONS
The tropical coastal Fish Poison Tree or Beach Barringtonia (Barringtonia racemosa) favours seasonally flooded rainforest sites and the tidal flats behind mangrove communities. The seed kernels, which are toxic, have been used for homicide and suicide in Papua New Guinea – while the fruit provided a poison for wild pigs in the Philippines (Perry & Metzger 1980; Webb 1948).
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In Thai medicine Barringtonia racemosa has been used as an antidotal remedy. Investigations have shown that extracts of this species, as well as Andrographis paniculata, had anti-scorpion venom activity, with a low cytotoxicity, supporting their efficacy as a venom antidote (Uawonggul 2006). Sri Lankan traditions have also used a decoction of the bark and leaves for treating rat and snakebites, rat poisoning, and as a remedy for boils. In addition, the seeds were regarded as being useful for itching skin conditions, piles, typhoid fever and gastric ulcers – with the bark similarly recommended for the latter (Deraniyagala 2003). The tree has also been utilised as a treatment for cancerous disorders in India. Seed extracts have shown experimental anti-tumour activity, with a low level of toxicity, that has suggested further serious investigations into its anticancer potential (Thomas 2002).
Table 7.2 Investigations into the Barringtonia genus that support their traditional medicinal uses Activity
Species: Investigations
Antimicrobial
Barringtonia acutangula • Root and leaf extracts have antibacterial properties against both gram-positive and gramnegative bacteria (Khan 2001). Good antimicrobial properties were exhibited by stem bark extracts, particularly against Bacillus subtilis and Aspergillus niger (Rahman 2005). • An evaluation of food and spice plants used in Thai traditional medicine for gastric disorders has shown interesting anti-Helicobacter potential for leaf extracts* (Bhamarapravati 2003). • Investigations of powdered seed extracts against urinary tract pathogens (Staphylococcus aureus, Pseudomonas aeruginosa, Klebsiella pneumoniae, Enterococcus faecalis and Escherichia coli), with some extracts showing very good activity (Sahoo 2008). Barringtonia asiatica • The tree contains gallic acid (a polyphenol) which has substantial antibacterial properties. • Studies of Barringtonia asiatica (leaves, fruits, seeds; stem and root barks) from Papua New Guinea have evaluated the antibacterial potential of the tree in great detail. The majority of the extracts showed a very good level of broad-spectrum antibacterial activity. • Fruit and seed extracts also possessed antifungal properties, primarily anti-candidal activity against Candida albicans. Stem-bark extracts were reasonably active against Aspergillus (Khan & Omoloso 2002). Barringtonia racemosa Extracts have shown good antimicrobial potential. • Bark extracts have shown significant antifungal activity, while extracts of the root (and the triterpenoid nasimalun A) have shown broad spectrum antibacterial properties (Deraniyagala 2003). • Leaf extracts: good antimycobacterial activity against Mycobacterium smegmatis. Potential for use as anti-tuberculosis agent (Mmushi 2009). • Leaf, stick and bark extracts: excellent antifungal (inhibitory) activity against a range of fungi, notably Fusarium sp. (leaf extract), Rhizophorus sp. (bark extract). • Phenolics (gallic and ferulic acids) and flavonoids (naringin, rutin, luteolin, kaempferol) were isolated (Hussin 2009).
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Anti-oxidant and antiinflammatory
Analgesic
Anticancer
Antidotal Antiparasitic and insecticidal activity
Neurological activity
Antidiabetic potential
Barringtonia racemosa • Bartogenic acid has shown anti-arthritic activity (Patil 2009). • Shoots and fruit extracts: high phenolic content which has been linked to good potential antioxidant activity (Razab & Abdul-Aziz 2010). • Anti-oxidant and anti-inflammatory activity of leaf extracts; active component identified as lycopene (Behbahani 2007). Barringtonia racemosa Bark extracts: analgesic (antinociceptive) activity that was of a rapid onset and a fairly long duration. This was possibly linked to its steroidal and phenolic components (Deraniyagala 2003). Barringtonia asiatica Extracts (various parts of the tree): contain gallic acid (a polyphenol) which has anticancer potential. The seeds of the Beach Barringtonia have shown a strong cytotoxic activity in anticancer investigations, as well as good antiviral activity (Yaplito 1992). Barringtonia racemosa Seed extracts: experimental anti-tumour activity, with a low level of toxicity (Thomas 2002) Barringtonia racemosa Anti-scorpion venom activity, with a low cytotoxicity (Uawonggul 2006). Barringtonia acutangula Leaf extracts: anthelmintic activity active against Indian earthworms; activity comparable with the conventional drug piperazine citrate (Padmavathi 2011). Barringtonia racemosa • Fruit (pericarp) and seed extracts: molluscicidal (Biomphalaria pfeifferi snails), cercaricidal (Schistosoma mansonii infection), antiplasmodial (chloroquine-sensitive Plasmodium falciparum), mosquito larvicidal (Anopheles arabiensis) (Ojewole 2005). • Triterpenoids, saponins, barringtogenol and barringtogenic acid identified as active principles of fruit and seed extracts (Ojewole 2005). • Stem bark also insecticidal. Barringtonia acutangula Extracts of the root and stem-bark had an interesting central nervous system depressant activity in mice. This sedative action would support its use in Indian medicine for psychiatric disorders (Satyavati 1976). Barringtonia acutangula • Root extracts have demonstrated ‘significant hypoglycaemic activity’ (Kapoor 1990). • Root extracts: antioxidant, anti-hyperlipidaemic and liver-protective activity in diabetic animals; significant benefits shown for overall lipid profile (Babre 2010a, 2010b). Barringtonia racemosa Enzyme-inhibition and anti-diabetic potential: • Recent investigations of bartogenic acid, isolated from the seeds (methanol extracts), has shown potent yeast and intestinal-glucosidase inhibitory activities, as well as amylase inhibitory properties (Gowri 2009, 2007). • Bartogenic acid is also present in the seeds of other species, i.e. Barringtonia asiatica (syn. B. speciosa) (Cambie 1986).
* The Helicobacter pylori bacterium is implicated in diverse gastric disorders – notably gastritis, dyspepsia, peptic ulcer disease and gastric cancer. This suggests that some traditional medicines may have a far greater preventive role in these disorders than has hitherto been appreciated (Bhamarapravati 2003).
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Cocky Apple
The Cocky Apple (Planchonia careya, formerly Careya australis). The short-lived filamentous blossoms of the Cocky Apple survive for only for a few hours. The flower opens at night or early in the morning for pollination. The fruit, which has been known as the Bush Mango or Wild Quince, is distinguished by a serrated-edged depression at one end with a single protruding whisker. The seedimpregnated yellow pulp can be eaten plucked straight from the tree – although if it is unripe (still white) it has an unpleasant astringent taste and irritates the mucous membranes of the mouth. The fruit can also be baked before use (Levitt 1981). Of the piscicidal properties of the Cocky Apple tree HamlynHarris and Smith (1916) commented: ‘This well known and effective fish-poison grows plentifully in forest country and along the foreshore of the Cardwell district … Its use is general in either fresh or salt water, but at Cardwell was resorted to when Cupania or Derris were unavailable.’ Joseph Maiden noted that
the Cocky Apple was a widespread tree of the Australian Myrtaceae: [It is] closely allied to the two preceding plants [Barringtonia racemosa and B. speciosa]. The bark was used by the aborigines of Cleveland Bay, Queensland, for stupefying fish, in fresh or salt water. I believe Murrell, a shipwrecked sailor, is the authority for this statement. Mr. E. Palmer, however, gives a little additional information when he states that the blacks on the Burdekin use the bark of the stem to poison fish in fresh water, and the bark of the root for salt water. There is probably a sufficient reason for this discrimination, and it would be well if some local resident would explain the matter (Maiden 1894).
At Dunk Island the bark from the base of trunk, as well as the root, was finely beaten to a mass before being thrown into a pool. The leaves
Burdekin River, near Ingham, in northern Queensland. Ludwig Leichhardt first sighted the river in 1845, naming it for Thomas Burdekin who helped to fund the expedition. (Courtesy: GNU, Gsolsen)
were also ‘accredited with medicinal virtue being beaten and applied as fomentations [warm poultice] (E.J. Banfield)’. The saponincontaining bark characteristically formed a soapy infusion in water (Cribb & Cribb 1981).
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• Tannin and saponin-based fish poisons were not the only major ichthyotoxins of medicinal importance. A major era of chemical and toxicological advancement accompanied the discovery of a compound known as rotenone. Indeed, plants containing rotenone were utilised throughout the tropics as fish poisons, a result of independent experimentation that gave quite consistent results wherever this occurred. Indeed, these plants were so effective that some Australian Derris species even acquired the names of ‘Wild Dynamite’ and ‘Poison Rope’. Those involved in the search for food, as well as the deployment of toxic plants, also stumbled across another major category of protein-based toxins. These
were found to be restricted to a few seed resources – notably the Gidgee Gidgee or Precatory Bean (Abrus precatorius) and the Castor oil plant (Ricinus communis). While many would be familiar with the presence of ‘Castor oil’ in old household medicine cabinets, few of us would truly appreciate the highly poisonous nature of the unprocessed seeds. Indeed the toxin responsible, which is known as ricin, as well as abrin from the Precatory Bean, are considered to be among the most virulent of those found in the Plant Kingdom. Their hazardous nature cannot be understated, although it can come as a surprise to find that these plants have been utilised medicinally – albeit only made possible with the discovery of some rather ingenious solutions. These stories involve the development of some of the most versatile, useful, and deadly, innovations from plant products known to man.
Chapter 8
DRUGS FROM ICHTHYOTOXINS
Derris trifoliata (image from Flora de Filipinas 1880–83, Francisco Manuel Blanco. Plate labelled as Pterocarpus diadelphus, Derris forsteriana, which are synonyms of Derris trifoliata)
Fish poisons or ichthyotoxins of particular potency were sourced from a number of the Fabaceae family 275
– notably Derris and Lonchocarpus – although there were other closely related genera with equally toxic properties, such as Millettia and Tephrosia. The efficacy of many of these plants was found to lie with very similar chemical components, which possessed rather interesting, and diverse, commercial potential. Another highly toxic vine in this family that was utilised as a fish poison is the Precatory Bean (Abrus precatorius). A toxin of a different class was isolated from the seeds, which had a rather nefarious reputation. Seeds of the Castor Oil plant (Ricinus communis) contained a very similar chemical – even though this weedy plant belongs to a completely different classification, the Euphorbiaceae. Many of the Fabaceae fish poisons were an economic choice because only a small amount was needed, at very low dilutions – and this made them much more efficacious than the tannin-based Eucalypt or Acacia fish poisons. However, despite the use of the word ‘poison’, these drugs aimed at stupefaction of the fish, rather than outright killing them. This was a much more desirable method of procurement because products with a high mortality rate also ran the risk of side-effects in humans. Derris, a genus that is widely distributed throughout the tropics, is one of the best-known ichthyotoxin resources. It contains a number of vines that were known to have particularly potent attributes. Overall there are around 40 species, with seven being found in Australia – and many traditions deployed their toxic potential wherever these plants were found. Aboriginal people were very familiar with the native representatives, the use of which was duly recorded by Joseph Maiden: ‘A leguminous shrub known to botanists as Derris uliginosa [now D. trifoliata] Benth., is found in Queensland and Northern Australia, and
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the pounded leaves are thrown into water, for the purpose of stupefying fish, by the natives of many tropical countries. No doubt this property was found out accidentally in the first place; – a broken bough fell into the water and it was noticed that the fish came to the surface.’
Poison Ropes and Wild Dynamite
Aboriginal fishing expedition, near Yirrkala, Northern Territory, Robert Miller 1948. American-Australian Scientific Expedition to Arnhem Land, Northern Territory, 1948.
Flowering Derris vine, mangrove swamp, Cairns, North Queensland. The Derris genus is generally composed of rainforest lianas or twining vines that climb into the forest canopy. The native species are: Derris elliptica, D. involuta, D. koolgibberah, D. rubrocalyx and D. trifoliata, plus a couple of undescribed Queensland species. The genus is found in the northern tropics (Queensland and the Northern Territory) ranging along the coastline to New South Wales. Derris trifoliata extends its distribution into the western Pacific as well as to eastern Africa.
Derris species found in Daintree, coastal habitat.
The toxicity of some Derris species was clearly evident, which quickly instigated investigations into their chemical activity: ‘The experiments … confirm the extreme utility and effectiveness of the plant as a stupefacient. The test fish, first evidencing considerable excitement, rapidly became stupefied and periodically rose to the surface. An infusion of one part of dried stem in one thousand parts of water proved fatal in under an hour. The rapidity of action it may be surmised, has earned for the plant the name of “Wild Dynamite” among the natives of Dunk Island’ (Hamlyn-Harris & Smith 1916). The scrub vine known as Poison Rope (Derris koolgibberah) had an equally toxic reputation. In the Ingham district, a local fish poison vine called buggera-buggera (identified as Derris uliginosa) was likewise effective. Early in the 1900s Inspector Sweetman of Townsville described the method of use by the local Aboriginal people: ‘The vine is cut up into two-feet lengths, sticks of about a finger’s thickness being preferred. They are beaten and bruised and handfuls thereof taken and thrown into the water, where they are again beaten and worked about. Fish quickly stupefy and, rising to the surface, are easily caught or speared. The method is only practicable in comparatively small waterholes. It is useless in running water, and acts better in fresh than in salt [water].’ Maiden made some interesting observations regarding a related species, detailing its use overseas: Derris elliptica Benth., is largely used in Java in fishing, and appears to be also a constituent of the Borneo arrow-
DRUGS FROM ICHYTHYOTOXINS
poison. Dr. Geshoff, of the Buitenzorg Botanic Garden [now Bogor Botanical Gardens, Java, Indonesia], has examined the plant. He finds that it has an exceedingly poisonous action on fish – a decoction of the roots being fatal, even when diluted to 300,000 parts of water. The only active constituent isolated is a resinous substance termed derrid, which does not contain nitrogen, and is not a glucoside; it readily dissolves in alcohol, ether, chloroform, and amyl alcohol, but is very sparingly soluble in water and potash solution … It occurs almost entirely in the cortex of the root, but has not yet been obtained pure. Its alcoholic solution has a slightly acid reaction and a sharp aromatic taste, causing a partial insensibility of the tongue, which remains for hours. A solution of 1 part in 5,000,000 is almost instantly fatal to fish (Maiden 1913).
The research that followed, leading to the isolation of pharmacologically active compounds such as rotenone from species of Derris, Lonchocarpus and Tephrosia, gave rise to the formulation of a range of insecticidal products for the international market.
Derris Insecticides
On the international market Derris came to be widely employed as an insecticide. The description in the 1949 British Pharmaceutical Codex (BPC) notes that this genus of tropical climbers was indigenous to ‘Burma, Siam, Cochin China, Malaya and the East Indian Archipelago, and [is] cultivated in Malaya, Singapore, Java, Sarawak, the Philippines, Tanganyika and the Belgian Congo’. Derris and Lonchocarpus contain highly variable amounts of rotenone, ranging
Derris involuta is found along the Queensland coastline, ranging into northern New South Wales. (Courtesy: www. noosasnativeplants.com.au)
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Derris seeds in pod.
from 3–20%, which means that although a large number of species contained the toxin, only a limited number of plants proved to be a viable resource. The levels in West African Derris and Lonchocarpus tended to be lower than in American or Indian species. Derris Preparata (Prepared Derris) was a powdered mixture of Derris and Lonchocarpus, ‘adjusted to the required strength, if necessary, by addition of fine powder prepared from derris or lonchocarpus of lower or higher rotenone content’. Officially, the drug was mainly sourced from Derris elliptica and D. malaccensis – although the BPC recognised that a number of other species were suitable for commercial use: ‘Among those that possess insecticidal properties or contain rotenone are Derris trifoliata (D. uliginosa), D. philippinensis, D. heptaphylla, D. polyantha, D. thyrsiflora, D. robusta, D. chinensis, and D. amazonica. The roots, rhizome and stem of D. trifoliata have been imported … It contains a much smaller proportion of active principle than either D. elliptica or D. malaccensis.’ Storage of the powder was an important consideration for maintaining the integrity of the raw material. Protection from moisture and light was essential to prevent deterioration of the active components – considerations that often have an underestimated influence on the activity of plant-based materials.
Nature’s Way Vegetable Dust Derris. (Courtesy: Yates Australia)
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Derris elliptica is a tropical species that is found in the Torres Strait Islands. This ‘Poison Vine’ has a widespread natural distribution throughout Asia (Myanmar, Bangladesh, Indochina, Thailand ) ranging to the Nicobar Islands (Indian Ocean), Malesia (but not Sulawesi, Borneo or the Moluccas), and some Pacific Islands (Hawaii). It is cultivated throughout its range – as well as in the Philippines, tropical Africa and America. The wild plant is low in rotenone (0.5%), while cultivated crops give a much hgher yield (12– 13%). The leaves are said to be highly poisonous, and the root powder is effective for removing predatory fish in fish ponds (www.worldagroforestrycentre.org). (Images courtesy Kim and Forest Starr, Hawaii)
Derris from the Extra Pharmacopoeia, Martindale, 1967.
DRUGS FROM ICHYTHYOTOXINS
A Hazardous Medicine
Derris trifoliata (formerly D. uliginosa) is found in the northern tropics (Queensland, Northern Territory) ranging to Papua New Guinea and Asia. This species contains reasonable amounts of rotenone.
Derris has rarely been utilised as a medicine due to its toxic potential. However, in Chinese traditions Derris trifoliata (powdered herb) could be made into a paste with wine and applied to traumatic injuries and rheumatic pain. However, it could only be used externally, and contact with open wounds was strictly avoided. The herb was also prepared as a wash for treating skin diseases such as eczema, itching (pruritus), ringworm and scabies. In Papua New Guinea, the crushed leaves of Derris elegans were mixed with green coconut water and the solution used as a wash for snakebite. The leaves of Derris trifoliata were also used used to ‘cool wounds’ (Holdsworth & Lacanienta 1981). Even so, the external use of Derris preparations was not without serious risk: ‘Prepared Derris … has been used in the treatment of scabies … in some cases this application may produce a burning sensation of the skin and an excoriating dermatitis which particularly affects the external genitalia. A similar dermatitis affecting the hands, arms, legs, thighs and genitals sometimes occurs in sensitive individuals from contact with derris powders’ (BPC 1949). Although most cases of accidental poisoning were mild due to the low doses involved, there have been incidents resulting in fairly serious toxicity. A report from French Guiana, which
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involved the use of an ichthyotoxic Lonchocarpus species in a suicide attempt by an 86-year-old woman, is illustrative. While rotenone has a low level of toxicity for humans when diluted, higher concentrations have neurotoxic potential. The woman initially experienced severe symptoms of digestive distress, followed quickly by loss of consciousness and respiratory insufficiency. She subsequently regained consciousness and resumed normal breathing within a few hours with only symptomatic treatment. Patients who survive the initial phase find that the condition improves fairly quickly (Chesneau 2009). Equally serious cases of accidental poisoning have occurred in children, who have inadvertently experimented with the plant or powdered derris dust – a situation with greater potential for fatalities. In addition to gastrointestinal distress (vomiting, stomach ache) and breathing difficulties (slow breathing), neurological symptoms include convulsions and muscle tremors. In severe cases, respiratory paralysis can lead to asphyxiation.
Derris trifoliata is a vine with a preference for sunny sites – usually along the edge of the rainforest, on creek banks, or mangrove forest waterways. It has a somewhat unusual characteristic flowering habit. The foliage produced during the current growing season does not develop flowers. The blossoms are found only on older growth areas of the vine – that is, near the base of the vine or on the stem.
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Rotenone from Lonchocarpus There are over 150 Lonchocarpus species native to tropical America, Africa, Australia and Madagascar. The West African or Yoruba Indigo, Lonchocarpus cyanescens, and L. laxiflorus are useful dye resources. Indigo (from the young leaves) has been widely used in African handicrafts (Abbiw 1990).
The British Pharmaceutical Codex of 1949 provided further details of the preparation and use of Lonchocarpus. It owed ‘its action to the presence of constituents similar to those of derris and it is used extensively in the same manner as derris in horticulture and agriculture. The fine powder, often mixed with talc, kaolin or finely ground gypsum, is applied to plants and animals as an insecticide or insect repellent, and mixtures of the powder, or of an extract, with soap solution, are used as a spray for similar purposes. Dilutions of derris and lonchocarpus powders, often containing less than 1 per cent. of rotenone, are usually described as “derris dust”.’ Commercial products were primarily sourced from Peru and Brazil, where Lonchocarpus utilis and L. urucu were the main species used. Recent analysis of rotenoids and flavonoids in Derris from Lonchocarpus urucu has confirmed it was an excellent source of these compounds, particularly rotenone, deguelin and rotenolone (Pereira 2000). It is of interest to note that, while many species have a low rotenone content, a number retain effective insecticidal properties, which suggests that there are other useful compounds present – these species include Lonchocarpus floribundus, L. rariflorus and L. sylvestris. In Nigeria, Yoruba Indigo (Lonchocarpus cyanescens) was employed as an anti-inflammatory and anti-arthritic remedy. Other treatments have recommended it for infantile constipation, seminal
insufficiency and venereal disease. The root has been employed as a wash to promote healing, including the sores that are associated with yaws – a nasty tropical skin infection due to a bacterium (Treponema pallidum pertenue) that is closely related to the syphilis bacterium (T. pallidum pallidum). Experimentally, the herb has shown effective anti-inflammatory properties that appeared to be linked to oleanolic acid derivatives and flavonoids (Iwu & Anyanwu 1982).
Bioactive Flavonoids
Lonchocarpus latifolius.
The Lonchocarpus and Derris genera contain flavonoid compounds with very interesting pharmacological properties (see also Table 8.1). Lonchocarpus latifolius root extracts contain diverse flavonoids including lanceolatin B, karanjin and pongamol. The latter two compounds, which are also present in Pongamia pinnata (syns P. glabra, Millettia pinnata) fruit extracts, have shown significant antihyperglycaemic activity (Dos Santos 2009; Tamrakar 2008; Magalhaes 2002,
DRUGS FROM ICHYTHYOTOXINS
2000; Mandal & Maity 1986). The antidiabetic activity of Derris indica root extracts were likewise linked to pongamol (Rangao Rao 2009). Pongamol and lanceolatin B are also present in Tephrosia purpurea and Lonchocarpus montanus (Magalhaes 2007; Chang 1997). Karanjin oil, from Pongamia pinnata seeds, contains karanjin and pongamol as the active components, with UV protective activity with potential for use as a sunscreen (Gore 2000). Karanjin has insecticidal and acaricidal (lice-killing) properties and is currently marketed as a bio-pesticide. Pongamia pinnata seeds. Concerns have been expressed regarding the cancerpromoting potential of rotenone-based insecticides. Despite the fact that initial studies mooted this possibility, subsequent investigations did not find any evidence of carcinogenesis (Greenman 1993; Gosalvez 1983). Strangely enough, a number of results have indicated quite the opposite. Leaf samples of one species, Derris sp. (cf koolgibberah), collected in Papua New Guinea, showed positive anticancer potential in CSIRO (Commonwealth Scientific and Industrial Research Organisation) investigations (Collins 1990). Rotenone extracts have demonstrated anti-carcinogenic properties in liver cancer studies in mice. This promoted research into the chemical pathways by which rotenone induced apoptosis in liver cells (Isenberg & Klaunig 2000; Khar 1999; Wang 1999; Cunningham 1995; Abdo 1988). Rotenoid compounds from Derris trifoliata have also shown interesting cancer chemopreventive (antitumour promotion) activity (Ito 2004a). In addition, anticancer activity was shown in studies of human colon cancer (adenocarcinoma) cells (Yoshitani 2001). Investigations of a product known as Cubè (a commercial rotenoid pesticide sourced from the root of Lonchocarpus) have likewise shown experimental anticancer potential that was attributed to a number
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of rotenoid compounds – e.g. rotenone, deguelin, pyribaden1 (Fang & Casida 1998; Rowlands & Casida 1998; Fang 1997; Gerhauser 1997; Udeani 1997). Anticancer investigations have also investigated the cytotoxic and anti-inflammatory potential of Lonchocarpus flavonoids and flavones (Cassidy & Setzer 2010; Liu 2009; Borges-Argáez 2007; Blatt 2002). In addition, there are a number of rotenoid compounds (deguelin, rotenone and its derivatives) that have shown potential for the modification of allergic reactions (Ashack 1980). 1 Lonchocarpus-based Cubè resins contain high levels of deguelin (ca. 21.2%), with smaller quantities of tephrosin (ca. 3.5%) and beta-rotenolone (ca. 3.0%). However, commercial formulations can vary considerably in their rotenoid content depending on the type of extract used in their preparation. In addition, rotenone and rotenoids are very sensitive to solar radiation (i.e. they suffer photodegradation), which significantly influences their storage stability (Cabizza 2004).
Rotenone-based Fish Poisons
Gyamkawa (Mundulea sericea) is a South African tree that has been utilised as a fish poison. It belongs to a rather widespread genus of 15 species that range from Africa, Madagascar and Mauritius to India, Sri Lanka and Papua New Guinea.
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There are a number of African plants in the Fabaceae family that have similar chemical components to Derris. They include the Matchbox Bean (Entada africana) and Gyamkawa (Mundulea sericea). These were also efficient insecticides (Oliver-Bever 1986). The bark and seeds of Mundula sericea contain rotenone and deguelin, although the tree appears to contain additional toxic components. It has been regarded as being more potent than the Vogel Tephrosia (Tephrosia vogelii), a wellknown and effective piscicidal plant. However, Gyamkawa has generally not been a popular choice because it kills the fish rather than merely stunning them and there is, therefore, an increased risk of poisoning from their culinary use. The bark was said to be potent enough to kill crocodiles – although those who were less optimistic believed that it would only ‘drive them away’ (Abbiw 1990). In some places the tree bark and leaves (sometimes the seeds and root) have been utilised as an arrow poison, as well as for suicidal and homicidal purposes. Interestingly, the leaves have been used by the Zulu as an emetic to treat
poisoning in people and dogs. Infusions of the root have also been recommended for infertility, and the powdered root to prevent miscarriage (www.plantzafrica.com). The fact that the incidence of Parkinson’s disease is higher in farmers using pesticidal agents has strongly suggested these compounds could be involved. Experimental evidence supports this, with rotenone and deguelin being linked to the development of neurological damage, although the effect of deguelin was only apparent at a higher dose (twice that of rotenone) (Caboni 2004). Recent investigations of the chemistry of Parkinson’s disease have even utilised rotenone as a neurotoxic agent in animal studies, focusing on the means by which brain damage and nervous dysfunction are induced in this disease. This research poses serious questions regarding the role of chronic pesticide exposure. The widespread use of the herbicide Paraquat has raised similar concerns (Chinopoulos & Adam-Vizi 2001; Hsieh 2001; Betarbet 2000; Lotharius & O’Malley 2000, Thiffault 2000; Greenamyre 1999).
Table 8.1 Medicinal uses and investigations of Derris and Lonchocarpus
Investigations into the chemistry of Derris and Lonchocarpus continue to discover new compounds of pharmacological interest. There appear to be few investigations (other than studies of their insecticidal value) that address the pharmacological activity of the Australian species. Certainly, this would appear to be a subject with some merit as various species have indicated potential molluscicidal, antimalarial, antibacterial and antifungal activity (Dos Santos 2000; Munoz 2000a, 2000b; Rai 1999; Blech 1991). Species Derris brevipes var. coriacea Derris elliptica Derris indica
Derris malaccensis
Derris scandens
Details (reference) Female antifertility remedy (India): mixture of powdered roots of Cassia occidentalis, Derris brevipes var. coriacea and Justicia simplex. Derris extracts showed significant anti-implantation and abortifacient activity. Weak oestrogenic activity (Badami 2003). Extracts demonstrated good antioxidant activity (Palasuwan 2005). High mosquito larvicidal activity of extracts (Komalamisra 2005). Antihyperglycaemic activity of the root extract: pongamol displayed potent intestinal alphaglucosidase inhibition (Ranga Rao 2009). Stem and root extracts contain flavonoids with anti-mycobacterial activity (Koysomboon 2006). Root bark extracts have shown good antibacterial activity (Khan 2006). Isoflavonoid pomiferin has shown strong anti-fungal and anti-oxidant activity; anticancer potential (cytotoxic and apoptosis-inducing activity towards human cholangiocarcinoma cells) (Svasti 2005). Root extracts: contain rotenoids with anti-Helicobacter pylori activity (Takashima 2002). Extracts had potent alpha-glucosidase inhibitory properties and moderate free radical scavenging activities (Rao 2007). Thai medicine: stem extract utilised as an anti-arthritic remedy; has shown anti-inflammatory and antioxidant activity due to isoflavonoids, notably genistein (Laupattarakasem 2004, 2003).
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Derris scandens
Derris trifoliata
Derris uliginosa Lonchocarpus araripensis
Lonchocarpus chiricanus Lonchocarpus cyanescens
Lonchocarpus montanus
Lonchocarpus neuroscapha Lonchocarpus sericeus
Lonchocarpus urucu Lonchocarpus utilis and L. urucu Lonchocarpus xuul Lonchocarpus xuul and L. oaxacensis
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Experimental immunostimulating activity in blood cell studies with potential for use in immune compromised conditions, e.g. HIV infection (Sriwanthana & Chavalittumrong 2001). Stem extracts: antimicrobial activity. Investigations have also indicated cardiovascular protential (hypotensive, lowering of the heart rate), although some isolated compounds (e.g. scandinal, scanderone, santal) have shown hypertensive activity. Various other compounds have been isolated of pharmacological interest – notably antioxidant (scandinone, derrisisoflavone A, santal) and antimicrobial properties against Staphylococcus aureus, including drug-resistant MRSA (lupalbigenin, derrisisoflavone A, santal) (Mahabusarakam 2004). Stem extracts: isoflavones tested for hypotensive activity (Rukachaisirikul 2002). Seed extract contained serine proteinase inhibitor with antiparasitic activity against the malaria protozoa (Bhattacharyya & Babu 2009). Stem extracts contain rotenoids with antioxidant and nitric oxide inhibitory activity (Tewtrakul 2009). Extracts have shown good antibacterial activity (Khan 2006). Root extracts had mosquito larvicidal activity (active components: rotenone and deguelin) (Yenesew 2005). Leaf extract has shown significant analgesic activity (Ahmed 2007). Lupeol from extracts attenuated allergic airway inflammation (Vasconcelos 2008). Extracts contain a flavone with gastroprotective activity (Campos 2008). Other flavonoid-containing species have shown gastroprotective activity (Reyes-Chilpa 2006). Root bark contains stilbenes with antifungal and mosquito larvicidal activity (Loset 2001). Anti-inflammatory and anti-arthritic remedy. Anti-inflammatory activity shown for root extracts (Iwu & Anyanwu 1982). Leaf for treating foot ulcers and as a skin dressing; stem and twigs or root infusion has been used after childbirth; root for leprosy, yaws; stomachic (with other medicines) and cataract (Ayensu 1978). Extract contains flavonoids (e.g. pongamol) with antimicrobial activity against Staphylococcus aureus, Bacillus subtilis and Cladosporium cladosporioides. Antifungal activity has also been demonstrated (Magalhães 2007). Root-bark extract contains chemicals with antineoplastic (cordoin, derricin and derivatives) and antibacterial activity (De Mello 1974). Anti-inflammatory (anti-oedema) activity of extract containing lonchocarpin and derricin (isolated from roots) (Fontenele 2009; Napimoga 2007). Seed lectin: inhibited the inflammatory response and the bacterial colonisation of infectious peritonitis in rats (Alencar 2005). Investigations have shown potential antimitotic activity of crude extract and the major constituents (e.g. derricin, lonchocarpin), but not antibacterial or haemolytic activity (Cunha 2003). Stem and twigs used as laxative for children; stem and twigs or bark used for convulsions, backache, parasitic skin diseases and eruptions; abdominal complaints; root applied to wounds and used as an antiscorbutic decoction; fruit considered poisonous in some areas (Ayensu 1978). Extracts demonstrated mosquito larvicidal activity (Gusmão 2002). Flavonoids and stilbenes isolated from an insecticidal resin of these plants (Fang & Casida 1999). Chalcones isolated from root extracts: selective trypanocidal activity of isocordoin derivatives (Borges-Argáez 2009). Flavonoids have been isolated from these Mexican species; jayacanol demonstrated antifungal properties against a wood-rotting fungus (Postia placenta) (Alavez-Solano 2000; Borges-Argaez 2000).
Malay Jewel Vine, Derris scandens, is a species from China, India, Malaysia and Indonesia. This vine has been utilised in Asian medical traditions as an expectorant, antitussive (to suppress coughing), diuretic, antidysentery and
analgesic agent. It is popular as a remedy for aches and pains, with a reputation for being useful as an antiarthritic herb. Clinical studies of its use in osteoarthritis tend to support these claims (Kuptniratsaikul 2011). The herb contains a number of compounds with potential as fumigation agents for pests that can contaminate stored products – notably osajin, scandinone, sphaerobioside, and genistein (Hymavathi 2011). (Image courtesy: JM Garg, India).
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Genus Millettia: Native Wisteria
Native Wisteria (Millettia megasperma); Ellis Rowan watercolour, 1887 (Source: National Library of Australia).
Millettia australis, Port Macquarie, New South Wales. In album: Botanical specimens collected and painted by Ida McComish F.R.G.S. in Australia, 1936–1956. (Part of the collection: Albums of water colour drawings of plants, birds and insects with botanical specimens.)
Millettia is a genus of trees and shrubs of the Fabaceae, some of which have a climbing habit. Australian species include Millettia australis, the Native Wisteria
M. megasperma, and a rare rainforest species from Northern Queensland, M. pilipes. The genus Millettia contains a number of species that have been utilised as fish poisons in Africa – M. auriculata, M. caffra, M. ichthyochtona, M. piscida and M. sericea. Doubtless Australian species have similar potential. The insecticidal compound rotenone is present in these plants – Millettia pachycarpa (1.2%) and M. ferruginea (rotenone 1%, as well as dehydrorotenone and tephrosin). While one would expect that their toxic properties rely on these components, the chemistry involved is somewhat more complex. Indeed, the kino (tannin-based resin) of the Native Wisteria, Millettia megasperma, is exceptionally tannin-rich (78%). This species, which has been a suspected stock poison, has also been responsible for poisoning soldiers who ate the raw pods (Webb 1948). The seeds of an Asian species, Millettia dasyphylla, were likewise poisonous if eaten raw although they were edible cooked (boiled or roasted) (Perry & Metzger 1980; Breyer-Brandwijk 1962; Webb 1948, Watt & Burkill 1935). A number of Millettia species have had a rather diverse medicinal reputation. In Africa Millettia grandis beans, which provided fish and arrow poisons, could be utilised (1–2 beans) as a vermifuge that was noted to be particularly effective for roundworms. The resin of the tree resembled Guaiacum – a medicinal resin with anti-inflammatory and anti-rheumatic activity. In Java Millettia sericea was recommended for intestinal worms – the powdered bark was taken in small doses. A few species also have an analgesic reputation. Millettia hemsleyana leaf (pounded) was applied locally as a remedy for toothache in Malaysia – as was the leaf of M. sericea. The latter, which has a fairly wide distribution from India to Papua New Guinea, was utilised as a fish poison in the Moluccas. In Malaysia the leaf decoction was taken as a febrifuge and diaphoretic (to induce perspiration in feverish conditions). The pounded leaves were poulticed on the ‘painful legs’ of animals (cattle and horses). The root had a reputation as a useful antiseptic for wounds, while the leaf decoction was recommended for urinary troubles and following childbirth. In Africa Millettia oblata root was also used as a bladder remedy (Perry & Metzger 1980; Watt & Breyer-Brandwijk 1962; Burkill 1935).
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Medicinal Millettia
The medicinal herb Ji Shui Teng can be sourced from Millettia dielsiana, M. reticulata or Spatholobus suberectus (Yeung 1985).
Millettia dielsiana and M. reticulata (stems) provide a Chinese herbal medicine that is utilised for invigorating blood circulation and as a blood tonic. This remedy illustrates the great clinical potential of the genus. It has been recommended for treating menstrual disorders (amenorrhoea, dysmenorrhoea), dizziness due to anaemia, arthritic pain, limb numbness, soreness of the back and knees – as well as for leucopenia (suppressed immunity) due to radiotherapy. Studies have shown uterine tonic properties of Millettia reticulata extracts, while M. dielsiana had an anti-arthritic, sedative and hypnotic effect in animal studies (Yeung 1985). Recent investigations of these species have isolated isoflavonoids with significant anti-inflammatory activity – and Millettia reticulata extracts have shown strong antioxidant and hepatoprotective activity (Hsu 2009; Gong 2009). Millettia speciosa has been likewise recommended for low back pain and rheumatism, as a tonic for sexual debility (nocturnal ejaculation in men or leucorrhoea in women), for treating chronic hepatitis and respiratory disorders (chronic bronchitis, dry cough, pulmonary tuberculosis)2 2 Millettia zechiana has been similarly utilised for rhino-pharyngeal and bronchial disorders on the Ivory Coast of Africa. The pounded bark was mixed with sea salt and Guinea grains and utilised as a gargle (Ayensu 1978).
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(Hong Kong CMRI 1984b). Millettia nitida is regarded as having similar anti-rheumatic, anti-arthritic, blood tonic and menstrualregulating attributes – the stems decocted or soaked in wine to make the remedy. To treat anaemia the herb was combined with eggs and red dates and prepared as a decoction (Hong Kong CMRI 1984a). The antimicrobial and insecticidal properties of the genus have inspired the use of a number of other species in folk medicine traditions. In India Millettia auriculata root was used for killing maggots in infected sores in cattle, while in Java M. sericea root juice was applied to neglected wounds in cattle and horses. The East African species Millettia eriocalyx has been utilised for treating skin eruptions, while in Taiwan the juice of M. reticulata stems was applied locally to wounds, and the root of M. taiwaniana for scabies. The latter was noted to contain rotenone and anhydroderrid (Perry & Metzger 1980). In Thailand the Mien people boiled Millettia extensa plants to make a wash for bathing scabies-infected skin and fungal problems such as ringworm (Anderson 1993). Certainly the pesticidal properties of rotenoid compounds would suggest that these could be quite effective remedies. Over the last decade research into the chemistry of the Millettia genus has isolated diverse compounds with anti-parasitic anti-cancer, oestrogenic, antiviral and anti-inflammatory potential: • Millettia thonningii: molluscicidal and cercaricidal properties of the powdered seeds. This species, which has been utilised as a purgative and anthelmintic remedy, has shown potential as a topical agent for treating or preventing Schistosomiasis infections. Isoflavones (alpinumisoflavone) and robustic acid were identified among the active components of the herb (Lyddiard 2002; Lyddiard & Whitfield 2001; Perrett 1995, 1994, Tang 1995; Squire & Whitfield 1989). • Millettia usaramensis subsp. usaramensis: contains rotenoids and isoflavonoids with activity against the malaria parasite, Plasmodium falciparum (Yenesew 2003).
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• Millettia pendula: extracts have demonstrated potent leishmanicidal activity (Takahashi 2004). • Millettia dura: rotenoids (deguelin, tephrosin) from the seeds were larvicidal against the Aedes aegypti mosquito (Yenesew 2003b). • Anticancer isoflavonoids are present in a number of species (Ito 2000): Millettia taiwaniana (Ito 2006a, 2004b), M. pervilleana (Palazzino 2003), M. pachyloba (Mai 2010), M. pachycarpa (Ye 2010), and M. brandisiana (Kikuchi 2009, 2007; Ishibashi & Ohtsuki 2008). Compounds named brandisianins from the latter have attracted particular interest (Pancharoen 2008). • Millettia reticulata: contains genistein, which has shown promising anticancer activity, as well as oestrogenic properties (Fang 2010).
• Isoflavones with hormonal activity: isoflavones (griffonianones) from Millettia griffoniana have likewise shown oestrogenic potential (Ketcha Wanda 2010; Wanda 2006, 2007) – as have extracts of M. conraui and M. drastica3 (Njamen 2008). However anti-oestrogenic isoflavonoids (millewanins, furowanin) have been found in Millettia pachycarpa (Ito 2006b). • Antiviral potential: in a study of 28 Asian herbs, Millettia pachycarpa showed strong antiHIV potential, as did Mallotus apelta (family Euphorbiaceae) (Ono 1989). Millettia leucantha also contains chalcones with moderate antiHerpes simplex activity (Phrutivorapongkul 2003). • Anti-inflammatory compounds, some of which have significant activity, have been found in: Millettia versicolor (a quinone), M. leucantha (a flavone), M. griffoniana (griffonianone D), M. brandisiana (toxicarol), M. dielsiana (isoflavonoids barbigerone, genistein) – with the latter also demonstrating anti-thrombase activity (Gong 2009; Pancharoen 2008; Phrutivorapongkul 2003; Fotsing 2003; Yankep 2003).
3 This study indicated that Nauclea latifolia and Bridelia ferruginea had similar oestrogenic potential (Njamen 2008).
The Indian Beech
Millettia pinnata.
The tropical Indian Beech (Millettia pinnata, syn. Pongamia pinnata, formerly P. glabra), is another native tree that has been traditionally utilised as a piscicide. Walter Roth (1901) recorded the following details of its preparation in northern Queensland: ‘After being roasted, the roots are beaten up on a stone, tied into bundles, and thrown into the water, which turns somewhat greenish: it is put in of an evening, and left there all night. Cooktown, Cape Bedford, and Princess Charlotte Bay.’ Indonesian tribes made similar use of it as a fish poison (Leaman 1991). Early investigations confirmed that all parts of the plant were toxic. Frogs poisoned with the extract died within 40 hours. Experiments showed that, like most saponin-based toxins, it was comparatively more poisonous to cold-blooded than to warmblooded animals. This meant that its toxic effects were not as severe in humans, who were more likely to experience vomiting. Joseph Maiden (1889) commented that it contained ‘a principle of great activity as an emetic’. However, in Indonesia the root infusion, which had a particularly potent reputation, has been used as a suicidal agent. The warmed potion was taken and the person was said to die while sleeping, although this did not always work as anticipated. There is an interesting record of a mismanaged suicide attempt by a man who was driven to despair by chronic dysentery that
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had lasted around three years. He fell asleep while warming the infusion and let it boil. After drinking the concentrated decoction he again fell into slumber, probably not expecting to survive the experience. One cannot doubt that when he woke up, cured of his affliction, he was somewhat surprised – and extraordinarily relieved. This potion would normally never have been utilised deliberately as an anti-dysenteric remedy. It was considered far too toxic (Leaman 1991). Indian Beech bark has also been used as an abortifacient in Vanuatu, and in Papua New Guinea the plant was reported to have anti-fertility properties (Cambie & Brewis 1997). Despite the toxic reputation of the root, in Papua New Guinea a remedy for diarrhoea and dysentery was prepared from the tops of the new leaves combined with sea water (Weiner 1985). The oil has had a more widespread reputation as a curative agent – being valued as an antiseptic, stimulant and healing remedy, with good antifungal and antibacterial properties. It was particularly useful for skin disorders (sores, ulceration, eczema, psoriasis, impetigo, ringworm), scabies, herpes – even leprotic sores and leucoderma (Kapoor 1993; Satyavati 1987).
Isoflavones and Hormonal Considerations
Legumes can act as sources of isoflavones with oestrogenic potential. In particular the isoflavones genistein and daidzein are found in Soybeans (Glycine max) and fermented soybean miso (Benlhabib 2002; Kaufman 1997). (Image courtesy: Andrew Grygus, theclovegarden.com)
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Concerns regarding the risks of side-effects such as cancer and heart disease that may be associated with hormonal replacement therapy (HRT) has encouraged research into natural alternatives. Soya (Glycine max) is one of the dietary legumes that contains saponins with weak oestrogenic activity. These isoflavones (genistin and daidzin)4 are chemically similar to oestradiol and have supportive potential for hormonal function. However, their effect is not straightforward and some consider that natural supplements have a more ‘balancing’ effect rather than acting as a straight-out oestrogenic agent. There can be substantial individual differences in the metabolism of the soy isoflavones, and this will significantly alter their efficacy in the body. In countries where soy-based foods form a substantial component of the diet women tend to suffer less acutely from menopausal discomfort (hot flushes, night sweats). Clinical studies have verified that soy-based supplements can alleviate menopausal symptoms in some individuals. A dose of around 60 g of soy protein provided 76 mg/day of soy isoflavones. Soy in the diet, as well as soy isoflavones (genistein, biochanin A), have been linked to a reduction in cancer risk, particularly breast cancer.5 Even so, the use of soy isoflavones in isolation may not be the best choice – and it would appear that dietary soy is the better alternative due to additional health benefits such as a lowered cholesterol levels and protection of bone integrity (Cho 2010; Ferrari 2009; Goodman 2009; Kwak 2009; Iwasaki 2008; Wu 2007; Trock 2006; Wayne 2001; Scambia 2000; Upmalis 2000; Zand 2000). Soybean isoflavones and the herb Pueraria lobata have shown anti-osteoporotic effects in animal studies. Some isoflavones, notably genistein and hypocotyl, have a potential for 4 Other flavonoids with experimental oestrogenic properties have been identified – i.e. luteolin and naringenin – while apigenin had progesterogenic activity (Zand 2000). 5 The inclusion of seaweed in the diet can also beneficially influence oestrogen and phytoestrogen metabolism. Seaweed contains soluble fibre that can influence colonic bacterial metabolism and bind to oestrogenic compounds, thereby facilitating their excretion (Teas 2009).
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Pueraria lobata, which is known as Ge Gen in Chinese herbal medicine, has traditionally been utilised as an antifebrile diaphoretic for feverish conditions, and as an anti-hypertensive agent in cardiovascular disorders.
preventing bone loss associated with estrogen deficiency, although the level of practical protection has been hotly debated. There may be some link to an antiinflammatory effect with the use of soy products. While there are studies suggesting that soy can be of practical value for some women wishing to avoid conventional hormonal replacement therapy, the use of individual isoflavones remains debatable, although genistein (and metabolites) appear to have the most potent effects. In general, dietary supplementation would seem to be preferential. However, oestogenic herbs should be avoided by individuals with problems due to oestrogen excess, oestrogenic-dependent tumours and on various oestrogenic drug supplements (Beavers 2010; Carmignani 2010; Gertz 2010; Ricci 2010; Taku 2010; Ferrari 2009; Wong 2009; Marini 2007; Wang 2004; Woo 2003; Wang 2003; Xue 2003; Zheng 2002). Isoflavonoids from the Southeast Asian species Pueraria mirifica have shown good oestrogenic activity – which may explain the reputation of this herb (Kwao Krua) as a ‘rejuvenative’ in Thai medicine. Clinically, the remedy was found to be useful in relieving menopausal symptoms (Cherdshewasart 2004; Lamlertkittikul & Chandeying 2004; Trisomboon 2004; Qi & Qi 2002; Lee 2002; Chansakaow 2000a, 2000b). In addition, Pueraria tuberosa (tuber) has been traditionally utilised in Indian Ayurvedic medicine as a contraceptive. Significant oestrogenic or progesteronic effects have been shown by the various extracts (Prakash 1985; Mathur 1984).
Kudzu
In Australia Kudzu, which is naturalised in parts of tropical Queensland and the Torres Straits, While
Kudzu (Pueraria montana var. lobata, syn. P. lobata) has excellent medicinal potential, the vine itself is an invasive weed, particularly in the USA, where it has rampantly spread throughout much of the southeastern part of the continent. Its presence is equally problem-atic in South Africa, New Zealand, and on some Oceanic Islands (notably Hawaii, Fiji and Vanuatu). (Image courtesy: Peggy Greb, USDA, Agriculture Research Service)
was probably an ancient food plant introduction to this part of the continent – where it does not appear to have the invasive qualities that have made it a nuisance elsewhere. This may be due to natural limitations imposed by environmental conditions or the plant may be genetically different (or even a different species or subspecies). In contrast, the vine has shown worrying pestilential potential further south along the eastern coastline. Outbreaks have occurred around Brisbane and Sydney and, although these have been rapidly dealt with, the weed has managed to become established in the Gold Coast hinterland. This is a matter of serious concern that has been compared to the environmental problems faced due to the import of another detested pest – the cane toad. (http://www.dpi.qld.gov.au/documents/ Biosecurity_EnvironmentalPests/IPA-KudzuRisk-Assessment.pdf (August 2008).
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Native Tephrosia
Tephrosia candida. (Courtesy: trees for the future, flickr)
A large number of species in the genus Tephrosia (around 54) are found in Australia – some of which have Asian links, including the White Tephrosia (Tephrosia candida), which ranges from the tropical Himalayas to Indochina and Indonesia. It possesses the insecticidal and piscicidal activities that are common to the genus. The plant also provides an excellent green manure as it has nitrogen-fixing properties. It has been widely used as a cover crop for plantations of coconuts, coffee, rubber and tea – as has the Vogel Tephrosia (Tephrosia vogelii). Both species have been listed as weeds in Australia, along with T. grandiflora, T. inandensis, T. nana, T. noctiflora and T. tinctoria (Lazarides 1997). On the Cape York Peninsula a shrub known as Te-Uma (Tephrosia rosea) held a reputation as one of the most effective piscicidal poisons known in the northern tropics. The leaves and stems were crushed and simply added to a waterhole and, unlike some other fish poisons, left the water drinkable after the harvest. In Western Australia Tephrosia phaeosperma roots, which were hammered to release the toxin, were wrapped in paperbark and the parcels placed under rocks where fish hide when the tide was out. Tephrosia supina and T. polyzyga are two other tropical native species with a similar reputation in the Northern Territory (Wightman 1994; Isaacs 1994; Smith 1993; Wightman & Smith 1989). Numerous species in Asia and Africa have a similar toxic reputation (Watt & Breyer-Brandwijk 1962):
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• A frican piscicides and insecticides: Tephrosia bracteolata, T. capensis, T. densiflora, T. diffusa (high insecticidal value), T. grandiflora (high insecticidal value), T. macropoda (high insecticidal value), T. nana (reputation equivalent to the Vogel Tephrosia), T. noctiflora, T. pedicellata, T. purpurea (low insecticidal activity), T. toxicaria (insecticide), T. vogelii (popular use as an insecticide). • Indian and Southeast Asian piscicides and insecticides: Tephrosia purpurea, T. toxicaria and T. candida; the seed of the latter was regarded as being a good insecticide, although root and stem preparations were said to be less potent than T. toxicaria or T. vogelii. • Species utilised as arrow poisons in Africa: Tephrosia capensis, T. densiflora, T. elegans, T. toxicaria and T. vogelii Tephrosia diffusa and T. macropoda were regarded as being highly poisonous, while T. lupinifolia root decoction was utilised in West Zambia: ‘for procuring abortion and for committing suicide. For the former, a decoction is drunk and said to kill the foetus. Uterine pains are said to come on in about ten hours. The poison is thought to be most effective during the first three months of pregnancy. In committing suicide, the pounded root is formed into a ball and inserted into the vagina. Considerable local and abdominal swelling develops within an hour or two of the application and death is said to follow with certainty in twelve to twenty-four hours’ (Watt & Breyer-Brandwijk 1962). Tephrosia vogelii had an equally poisonous reputation. The root (mixed with crocodile or snake bile) was also utilised homicidally, as well as for suicide, and to procure abortion. Tephrosia densiflora and T. vogelii have likewise been employed as abortifacients (Watt & Breyer-Brandwijk 1962). In contrast, a few species were utilised medicinally – the infusion taken following childbirth, probably for a cleansing or tonic effect: Tephrosia linearis, T. noctiflora and T. nubia (Dzenda 2008; Burkill 1995). In Tangyanika the aromatic root of Tephrosia atroviolacea was utilised similarly, the root pounded and mixed with sweetened mealie meal porridge (Watt & Breyer-Brandwijk 1962). Early Australian experiments evaluating Tephrosia rosea and T. purpurea demonstrated substantial toxicity: ‘when a fish is placed in a dilute solution it shows a
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great excitement at first but soon becomes quiet. The fins lose colour and become paralysed and the fish turns over and eventually dies.’ The researchers concluded that Tephrosia rosea was a extremely efficacious. Even minor concentrations were potent: ‘Concerning the toxicity of the final product there can be no doubt; a concentration approximately 1:1,000,000 proved fatal to test fish in half an hour’ (Hamlyn-Harris & Smith 1916). This activity was similar to that of a couple of well-known African species: Tephrosia macropoda6 and the Vogel Tephrosia (Tephrosia vogelii). The leaves and small branches of the Vogel Tephrosia were typically beaten to a pulp and thrown in the water, where it induced temporary paralysis in the fish which were then easily collected. However, mention was made of a rather unusual side-effect experienced by the fish harvesters. Their skin developed a toughened characteristic: ‘a person wading in the poisoned water, in connection with catching the fish, generally complains of either a dead feeling in the legs or of roughness of the skin’ (Watt & Breyer-Brandwijk 1962). The potency of this species has been confirmed by researchers in Gabon. Even with exposure to high temperatures (boiling for 90 minutes), leaf extracts retained their activity at a high dose, although weak doses were much less effective (Ibrahim 2000). Native to Africa, Madagascar and Mauritius, the Vogel Tephrosia (Tephrosia vogelii) is now found
Tephrosia vogelii. (Courtesy: Paul Latham, flickr) 6 The crushed root of this species was fatal to fish in one hour at a concentration of 1:25,000,000 in water. It also has useful molluscicidal and parasiticidal properties (Watt & Breyer-Bandwijk 1962). Tephrosia uniflora is another African species with molluscicidal potential (Adewunmi & Sofowora 1980).
throughout the tropics. It has been widely cultivated for commercial rotenone production and is a particularly useful crop that can be harvested after only six months. In comparison, Derris and Lonchocarpus crops take two to three years before a harvest is feasible (Duke & duCelliar 1993). Tephrosia vogelii has long been regarded as a potent toxin with substantial pesticidal properties, as well as being utilised as a purgative, emetic and anthelmintic (worm removal) agent. It has notable efficacy as an insecticide against lice, fleas and ticks. The leaf has also shown useful molluscicidal properties (i.e. a good level of activity against snails that are vectors for diverse parasitic diseases) (Duke & duCelliar 1993). In addition to the widespread use of the plant (bark, leaf, unripe fruit) as an abortifacient, a leaf-based water extract was taken in Cameroon as an emmenagogue (to induce the menses). The sap has been added to palm wine for use as an antidiarrhoeal agent, while the root scrapings were applied to a toothache. There are some traditional recommendations that suggest that the herb has antimicrobial properties – for example, it was used in Tanzania for earache (pulped leaves and sap used locally), as well as for tuberculosis and as a bactericidal agent in Angola (Dzenda 2008). Investigations of dried fruit extracts have shown weak antibacterial activity against Staphylococcus aureus; weak antiviral activity against the measles virus; and strong antifungal activity against Microsporum canis (which is responsible for tinea/ringworm infections) – although activity against a similar fungal pathogen, Trichophyton mentagrophytes, was weak7 (Vlietinck 1993). This lends some support to the traditional use of the root infusion in fungal foot infections. In addition the plant has been utilised as a bone-setting agent. The ground leaves and stem bark were mixed with vegetable oil and rubbed around the area of a fracture, while pieces of the cut stem acted as splints (Ekpendu 1998). Tephrosia macropoda, which has a toxic reputation similar to that of Vogel’s Tephrosia, has been utilised as an antiseptic, anthelmintic and febrifuge. In feverish conditions (including typhoid) the unburnt inner root portion was taken with Bopusia scabra (inner root bark). Charring the root and utilising the unburnt 7 A related species, Tephrosia villosa, contains antimicrobial peptides known as defensins with potent, but selective, antifungal activity (Vijayan 2008).
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inner potion was thought to reduce its toxicity. This species has good pesticidal properties and a root decoction (sometimes a paste of the powdered root) was employed as a hair wash. Tephrosia diffusa was used similarly. However, the insecticidal activity of Tephrosia macropoda can vary, with some strains of the plant having a superior effect. Although utilised medicinally, the root decoction contains a cardiac toxin and has been responsible for fatalities (Watt & Breyer-Brandwijk 1962). There are a number of other Tephrosia species that have been of toxicological or medicinal interest: • Tephrosia aequilata8 (Africa): used by the Haya for the relief of abdominal pain by sniffing plant or rubbing on abdomen (Watt & Breyer-Brandwijk 1962). • Tephrosia bracteolata (Africa): Tanzania – root taken by pregnant women suffering syphilis (Watt & Breyer-Brandwijk 1962). • Tephrosia capensis (Africa): Zulu use warm root infusion as an emetic for biliousness; Southern Sotho employed cooked root for palpitations, and
Derris purpurea var. purpurea. (Courtesy: Kim and Forest Starr, Hawaii) 8 This name has been used as a synonym for Tephrosia vogelii (Daenda 2008)
• • •
• • • •
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plant decoction was combined with Commelina africana to treat ‘weak heart’ and nervousness (Watt & Breyer-Brandwijk 1962). Tephrosia densiflora (Africa): used against skin disorders (Oliver 1960). Tephrosia kraussiana (Africa): warmed root infusion used by Zulu to treat troublesome night cough (Watt & Breyer-Brandwijk 1962). Tephrosia lucida (Africa): to attract the opposite sex a cold root infusion was made with Dianthus crenatus and the face washed with the froth: ‘the infusion is sometimes drunk as an emetic to assist this good work’ (Watt & Breyer-Brandwijk 1962) Tephrosia nana (Africa): Nigerian Igbo people use the parched leaf (ground) to treat yaws (Burkill 1995). Tephrosia pedicillata (Sudan): root chewed for throat and lung complaints (Burkill 1985). Tephrosia petrosa (India): boiled leaf eaten and is considered good against syphilis (Chopra 1956). Tephrosia pumila (Papua New Guinea): plant used to relieve fevers – it is boiled (decocted) and the patient wrapped in a blanket. They perspire in the vapour which is also inhaled (Holdsworth & Lacanienta 1981).
Tephrosia purpurea (Wild Indigo) is found in northern Australia, ranging throughout Queensland and the Northern Territory, and in the north of Western Australia. Despite its fairly widespread distribution there are no records regarding its use by Aboriginal people. It is likely to have been utilised for treating skin disorders similar to the deployment of Tephrosia oblongata for scabies in the Northern Territory – the inner bark heated in water and the affected site daubed with the decoction. The tuber of another unnamed native species, crushed and boiled, were also utilised as a wash on skin sores to promote healing (Barr 1993). Perhaps other species were utilised similarly although, unfortunately, there is a distinct paucity of information regarding many of the medicinal species that are found on this continent. (Image courtesy: JM Garg, Wikipedia)
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(Right) Tephrosia filipes is an Australian species with a wide distribution across the northern tropics, extending from Western Australia to Cape York. It can be found ranging south to Brisbane and northern New South Wales. (Courtesy: KAW Williams, Native Plants of Queensland, Vol. 2)
Table 8.2 Medicinal uses of Tephrosia purpurea (Note: for a recent review of Tephrosia phytochemistry see Dzenda 2008.) Country Africa
Medicinal uses (source) Nigeria: diuretic, blood purification; coughing and colds; gargle (Ainslie 1937). Tanzania: slightly burnt root chewed for stomach pain; root and leaf have emetic qualities (Burkill 1995). Senegal: many medicinal uses: diarrhoea and whooping cough in children; vaginal douche; adult diarrhoea; spasmodic cough; fevers; sterility, rickets and syphilis (Kerharo & Adam 1964)
India and Pakistan
Cardiovascular Tephrosia used for treating for cardiac disorders including heart failure (Sajid 1996; Rao 1984)
India
Dried herb: tonic, laxative, diuretic, deobstruent, antiinflammatory, antibacterial (Jain 2009; Lodhi 2006; Rastogi & Mechrottra 1990; Chada 1976). Respiratory tract: dried herb: treatment of respiratory problems (cough, bronchitis, asthma), kidney disorders and bilious febrile attacks. Healing agent: • Dried herb: external application: boils, pimples, bleeding piles. • Seed: edible and yields an oil: external application to scabies, itching, eczema, skin conditions. Other: seed pod extract effective for pain, inflammation; decoction used as anti-emetic (stop vomiting),
Supportive investigations (source) Immune system • Flavonoidal fraction has shown immunomodulatory properties (Damre 2003). • Anti-allergic potential (Gokhale & Saraf 2000). • Root extract: experimental protective effect against bronchoconstriction and anaphylaxis (Deshpande 2008). Antiviral Flavonoids from the genus (glabranine and methylglabranine from Mexican species) exert an antiviral effect on the dengue virus (Sanchez 2000). Cardiovascular activity • Dose-dependent hypotensive activity of Tephrosia purpurea leaf extract in dogs reported (Rao 1984). • Tephrosia uniflora: force of cardiac contraction and coronary outflow were appreciably reduced; heart rate was virtually unaffected (Sajid 1996). • Cardiac glycosides have been isolated from T. candida leaves (Sajid 1996). Wound healing Studies have shown wound healing, antioxidant and antibacterial activity of plant extracts; a flavonoid-based ointment preparation has shown excellent wound healing activity (Lodhi 2006 & 2010). Anti-inflammatory Plant extract showed significant antiinflammatory effect in subacute inflammation, but not active in acute inflammation (Shenoy 2010). Anti-inflammatory and antibacterial Chewing roots has shown excellent clinical results for treating tonsillitis (Karnick & Parhak 1983).
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India
Genito-urinary disorders: seed decoction: dysuria, urine retention (Sharma & Sharma 1997). Other: plant: impotence, gonorrhoea, diarrhoea, rheumatism, ulcers; disorders of heart and blood (Jain 2009). Skin disorders: roots: treatment of leprous lesions; juice used to treat skin eruptions (Jain 2009). Injury: leaves are pounded with castor oil to make a paste which is applied to treat sprains (Vijayakumar & Pullaiah 1998). Gastrointestinal pain: root juice mixed with hot water and taken to ease stomach pain (Vijayakumar & Pullaiah 1998).
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Antimicrobial • Root contains an anti-mycobacterial phytosiderophore* active against Mycobacterium tuberculosis (Rajiv 2001). • Root extracts showed good activity against Proprionibacterium acnes indicating usefulness for treating acne (Kumar 2007). • Root extracts showed very good antifungal activity against Aspergillus niger and Candida albicans (Gupta 2008). • Root extracts: antibacterial activity against gramnegative and gram-positive bacteria (a higher level of activity demonstrated against the latter) (Gupta 2008). Antimicrobial and anticancer • Extracts possess antibacterial activity; flavonoids have shown antimicrobial properties. • Plant extract reported to have experimental anticancer activity (Jain 2009). Flavonoids, biological activity • Rutin (1.913 mg/100 g) and quercetin (0.473 mg/100 g) in plant extracts: flavonoids have anti-allergic, anti-inflammatory, anti-thrombotic, vasoprotective properties; inhibition of tumour promotion and gastroprotective activity (Jain 2009). • Flavonoids (tephrorins A and B, tephrosone) isolated with anticancer potential (Chang 2000).
India
Plant: tonic, laxative, used as anthelmintic for children; taken internally for blood purification; considered a cordial (Chopra 1956). Gastrointestinal • Fresh root bark: ground and made into pills, with a little black pepper for obstinate colic (Chopra 1956). Root: bitter, given in tympanitis, dyspepsia and • chronic diarrhoea (Chopra 1956). • Traditional use in India for treatment of wounds including gastroduodenal ulceration (Chinniah 2009).
Tonic, laxative, antipyretic; anthelmintic, alterative, diuretic, deobstruent** (Kapoor 1990). Digestive and respiratory tracts Root: diaphoretic and bitter, used in dyspepsia, chronic diarrhoea, bronchitis, asthma, inflammation. Skin healing Seed oil: very effective for skin disorders including eczema. Liver disorders Plant used for treating liver and spleen disorders in India. An important component of hepatoprotective herbal formulations, e.g. Tephroli and Yakrifit (Jain 2009).
Anti-diabetic potential • Seed extract has shown antioxidant and hypoglycaemic properties. • Leaf extract has shown anti-hyperglycaemic and antihyperlipidaemic activity in diabetic rats (Pavana 2007, 2008; Rahman 1985). Gastrointestinal disorders • Extracts demonstrated activity against Helicobacter pylori (including metronidazole-resistant strains), with synergistic potential for combination with antibiotics (Chinniah 2009). • Extracts were active in acidic environment, resembling conditions found in the stomach (Chinniah 2009). • Root extract: cytoprotective, gastroprotective activity in stomach and duodenal ulcer (Deshpande (2003). • Fresh root juice antimicrobial (Deshpande (2003).
Hepatoprotective and anticancer • Hepatoprotective activity shown by extracts (aerial parts) against thioacetamide-induced liver. Hepatoprotective against CCl4 (carbon tetrachloride) damage comparable to silymarin(Khatri 2009). • Active components may be the polyphenols and flavonoids that are present in extracts (Sangeetha & Krishnakumari 2010; Jain 2006). Related species • Tephrosia calophylla root extract has shown similar hepatoprotective activity (Adinarayana 2011). • T. toxicaria: flavonoids with cancer chemopreventive activity against hepatoma cells (liver cancer) isolated from stem extracts (Jang 2003).
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India (cont’d)
Fiji
Healing agent Plant used for earache treatment. Leaves used with those of Acacia richii: crushed, sundried and mixed with water to make a wash for treating scabies (Cambie 1994).
Anticancer • Studies have shown strong skin antioxidant activity; significant reduction in the skin tumor-promoting effect of croton oil (Khan 2001; Saleem 2001). • Potent chemopreventive agent against renal oxidative stress (renoprotective) and experimental carcinogenesis (Khan 2001; Saleem 2001). Biological components Rotenoids, amino acids, and isoflavones. Plant also contains diverse flavonoids, notably rutin. Leaves contain β-sitosterol, lupeol, rutin and an alkaloid. Fresh flowers contain anthocyanidins (Cambie 1994).
* Phytosiderophores act to remove iron from the site of an infection thereby inhibiting pathogen growth. These compounds have been of interest for therapeutic purposes where removing iron from the blood is necessary – e.g. in conditions such as thalassaemia (Rajiv 2001). This suggests they may also be useful for haemochromatosis – although Aloe Vera juice (99% pure) is highly effective as a clinical agent for chelating iron from the blood in the latter condition (personal experience). ** A remedy that removes ‘obstructions’, often used to clear or open body channels – usually used to enhance movement of fluids or secretions along natural channels, e.g. open the sinus passages, enhance sweating or clear the ur
An Antirheumatic Wild Bean? The Wild Bean (Tephrosia varians), one of the Australian fish-poison plants, was used in the treatment of rheumatism by early settlers. Some interesting incidents were bound to occur in the experimentation with the local flora, and sometimes the results could be fortuitous. Matthew Butler JP recounted one such story of an old man who thought he was dying of rheumatism: On the 24th December, 1894, I was sent for to make the will of an old man who was, as he thought, dying from rheumatism. In a fit of abstraction he pulled up the root [Tephrosia varians] and ate it. Fancying it gave him relief, he pulled more, boiled it and drank the liquor. Within a week there was a marked change in him, and now he is quite well and looks ten years younger. A miner, who has been suffering for over two years from a scrofulous [glandular swelling] affection took a decoction of this root for a fortnight, and his skin seems now perfectly clear, and he tells me he feels a new man. I had a light touch of rheumatism in the leg and tried a decoction of the root with the result that the pain has gone and the stiffness is wearing away (quoted in Lauterer 1897).
Over a century later Tephrosia varians has been utilised clinically by Dr Wojciech Kielczynski in Australia for treating arthritic pain with good results. Patients were able to substantially
reduce their reliance on NSAIDs or analgesics by the use of the tincture internally and externally (Kielczynski 1997). Certainly investigations into the pharmacology of Tephrosia purpurea support the anti-inflammatory, antioixidant and analgesic properties of the genus. Joseph Lauterer investigated a sample of the root (under the genus name Galactia), which was: ‘three to four inches long, grey outside, yellow like a turnip inside, is destitute of a peculiar smell, but has an acrid taste which made me suspect saponin in the drug. On further examination I found the root to contain neither saponin, nor any alkaloid or glucoside, but to be full of a sticky acrid yellow resin to the amount of thirty per cent. of the whole weight of dry root.’ He determined that: ‘Galactia resin is chemically related to the Guaiacum resin, and therapeutically it comes near the same. Galactia resin might be recommended in rheumatism, skin diseases, scrofulosis and syphilis, and in rheumatism, and skin diseases it might surpass guaiacum in quickness and certainty of effect.’ Guaiacum (Guaiacum officinale) wood, resin and bark were once widely used for the treatment of these disorders. In particular it had a great reputation in the sixteenth century as a cure for syphilis, and was used for this purpose into the early twentieth century.
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The Poisonous Precatory Bean
Abrus precatorius seeds.
Abrus precatorius, from Koehler’s Medicinal Plants, 1887.
The Precatory Bean, Abrus precatorius, belongs to one of the largest plant families, the Pea or Bean family (Fabaceae, formerly Leguminosae) – although the genus Abrus is small, with around 13–18 species that are mainly of African origins. Other species tend to have a restricted distribution in Somalia, Madagascar, Zaire, India, Saudi Arabia (and Yemen), Vietnam and Laos. Abrus precatorius is the most familiar and widespread, ranging throughout the tropics from Africa to India, China, Oceania and Australia, although it appears to have originated in Southeast Asia. The explorer Ludwig Leichhardt recorded one of the earliest encounters with the vine in Australia: ‘On the rocky crest of the hill, I gathered the pretty red and black seeds of a leguminous climbing shrub’. In 1882 the Reverend Tenison-Woods described it from the
The Precatory Bean (Abrus precatorius) has been known as the Rosary Pea, Jequirity, Indian Liquorice and Gidgee Gidgee. The botanical name Abrus refers to a Greek term for ‘graceful’, alluding to the flowers, while precatorius is derived from the Latin precor, ‘to pray’, referring to the use of the seeds used as rosary beads. The white, pink or mauvecoloured blossoms appear during January to March, after which the long-lived seed pods remain on the vine until the end of the year. They split when mature to reveal distinctive bright red, black-spotted ‘crab’s-eye’ seeds. Initially a slender climbing vine, the plant matures into a thick and woody liana. (Image courtesy: Kim and Forest Starr, Hawaii)
tropical northern-eastern coast: ‘Another world-wide tropical species found in all the jungle close to the sea from Rockhampton to Cape York. Every one must be familiar with the brilliant scarlet and black seeds which are so often brought as curiosities from the East and West Indies, and used as beads, ornaments for boxes,
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&c.’ Surprisingly, these men appear to have been quite unaware of the danger posed by these pretty decorations! The plant tended to gain a rather notorious reputation wherever it grew. However, processing techniques can alter the degree of toxicity, and the use of the seed (or ‘bean’) or the bark must be clearly differentiated from that of the vine foliage. African dance mask decorated with Abrus precatorius seeds. Aboriginal people were (Courtesy: The Spurlock aware of the vine’s Museum, University of Illinois toxicity and employed at Urbana-Champaign) the bark as a fish poison, merely pounding it then washing it in small waterholes. However, extreme care was taken to prevent the sap gaining access to the bloodstream via cuts or scratches. While the poisonous effects of the bark were unmistakable, that of the seeds was less obvious. This was because the hard seedcoat kept the poison contained and its toxic potential only became evident if the coating was breached. Henry Burkill mentioned that the seeds had been utilised with murderous intent in India: ‘Criminal poisoning of cattle by administering the seeds has been not uncommon in India; but the skilful poisoner makes more sure of success by making a short spindle of pounded Abrus seeds and forcing them into a wound in the skin. Gautier (Les toxines microbiennes, 1896) states that one-hundredth part of the amount necessary for poisoning by the mouth suffices for poisoning if placed under the skin.’ In West Africa the Precatory Bean had a similarly dangerous reputation that led to its deliberate use as an ordeal poison. In a 1957 review of The Ordeal Poisons of Madagascar and Africa, GL Robb commented: ‘although the use of this plant as an ordeal poison was widespread, there were certain hindrances to its continued popularity as anything more than an accessory instrument. One drawback was that it possessed the characteristic toxalbumin
latent period before the commencement of effects. This was due to its partial inactivation by gastric juices, resulting in slow absorption.’ The fact that the seed could be swallowed entire without toxicity was another impediment to its use as an ordeal poison. Those overseeing the procedure needed to ensure that the participants chewed vigorously to get the best results.
A Bitter-sweet Medicine
Despite the toxic reputation of its seeds, the vine has had both culinary and medicinal uses. In Australia colonists once harvested the plant as a form of ‘Wild Liquorice’. It was also infused to make tea, although it did not have the aromatic flavour of true tea and has been described as tasting ‘like grass clippings’ (Low 1992). Since ancient times the roots and leaves were used in Southeast Asia in a manner similar to Liquorice. The drug was mentioned in an Indian Sanskrit medical work as long ago as 600 AD. The plant has provided a liquorice substitute in Malaysia, India and Indonesia due to the small amounts of a sweet component, glycyrrhizin, which it contains. Opinions differ with regard to the sweetening qualities of the various parts of the plant (leaves, stem and root) and how its glycyrrhizin content compares to that of Liquorice (Glycyrrhiza glabra).9 The leaves can contain up to 6–10 per cent of this compound and are considerably sweeter than the root, although they can have a somewhat pungent aftertaste. The fact that other sweet-tasting non-toxic glycosides (abrusosides) that are 30–100 times sweeter than sucrose are present in the leaves would certainly affect its appeal (Choi 1989; Oliver-Bever 1986). Widely known as Jequirity leaf, the leaf of Abrus precatorius has mucilaginous properties that were useful for the treatment of a wide variety of disorders. They were chewed or made into a decoction for respiratory problems: to relieve hoarseness, coughing or bronchial constriction. The decoction was also utilised as a remedy for constipation, gastrointestinal colic, and for general pain relief. In part, the herb’s efficacy may be explained by its glycyrrhizin content, as this compound has substantial anti-inflammatory, expectorant, anti-tussive, and antibiotic activity. 9 Abrus has been cultivated in France as a source of glycyrrhizin.
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Jequirity leaf tea has been a common beverage in Jamaica. In Tobago the leaf infusion was taken as a remedy for diabetes, hypertension, cramps and colds (Seaforth 1998).
However, the use of fairly large doses of glycyrrhizin, taken over a long time, can cause fluid retention. This is due to the development of a metabolic disturbance that is linked to the retention of sodium and chloride, associated with increased potassium excretion – effects that are similar to those induced by cortisone. Therefore the long-term use of herbs that contain glycyrrhizin should be attended with some care and good professional advice (Iwu 1993; Oliver-Bever 1986; Perry & Metzger 1980; Quisumbing 1951; Burkill 1935).
Liquorice: An Ancient Herb of Extraordinary Value
The sweetening agent glycyrrhizin (a triterpene saponin), which is around 50 times as sweet as sugar, is a natural mixture of the potassium and calcium salts of glycyrrhizic acid. Glycyrrhizin and its sapogenin, glycyrrhetinic acid, have significant pharmaceutical properties (Nassiri Asl & Hosseinzadeh 2008). In Japan glycyrrhizin (known as SNMC: Stronger NeoMinophagen C) has been used for over 60 years with excellent clinical results as an anti-allergic and antidotal agent. It was later found to be highly effective in the treatment of hepatitis, for which it has been used for the last 30 years. Glycyrrhizin has also shown impressive antiviral properties, with good clinical applications for AIDS patients. In addition, Liquorice contains a substantial diversity of phenolic components (around 70 10 Overall around 300 different phenolic compounds have been isolated from the roots of various Glycyrrhiza species: G. glabra (70), G. uralensis (60), G. inflata (60), G. aspera (40), G. eurycarpa (40), G. pallida (30) (Shibata 2000). As there are around 30 species in the genus, this suggests that many more compounds probably remain undiscovered.
Glycyrrhiza glabra, from Koehler’s Medicinal Plants, 1887.
different compounds10), some of which have substantial medicinal potential, notable among them being isoliquiritigenin, with antispasmodic, anti-tumour activity and antidiabetic potential. Licochalcones have shown anti-inflammatory, anti-HIV, anti-tumour activity – with additional anti-malarial and anti-Leishmania potential (Shibata 2000). Understanding the activity of these compounds is all the more imperative as their total synthesis is difficult (maybe impossible) due to a unique structural chemical complexity that is very closely linked to their biological activity. They can, however, be employed as the starting compounds for chemical modifications that aim to enhance drug effects. For instance, the development of deoxoglycyrrhetol was accompanied by a remarkable enhancement of antiinflammatory, anti-allergic and anti-ulcer activity (Shibata 2000). The drug carbenoxolone, which is a synthetic derivative of glycyrrhetinic acid, has been in clinical use in Western medicine (UK, USA) as an anti-ulcer and anti-inflammatory medication for the treatment of gastric and oesophageal ulceration, gastric reflux and mouth ulceration. The drug has
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a mucoprotective effect, although its use has been limited by metabolic problems with potassium and sodium (treatbacteria.com/tag/carbenoxolone). Later studies suggested the drug also has beneficial effects on verbal memory (Pilcher 2004). While the system of modern drug development is far from perfect, this certainly illustrates the remarkable potential of an age-old herbal medicine. The research supports the extraordinary properties of the herb itself, with a greater understanding of its chemistry lending greater validity to the traditional uses of Liquorice.
Glycyrrhizin is present at high levels in Liquorice root: 4–5 per cent of the dried root. The total flavonoid content of the root is 1–2 per cent. Around 50 different triterpene saponins and sapogenins have been isolated from various species in the genus (Shibata 2000). Overall, the levels of triterpenoid saponin in Liquorice root may be quite high (4– 20%) (Asl & Hosseinzadeh 2008). An interesting find is that the characteristic taste of Liquorice is extraordinarily stable – with material stored for 1200 years retaining glycyrrhizin and its sweet flavour (Shibata 2000).
The elongated root of Abrus precatorius has been used as also been used as a demulcent flavouring agent. The Reverend GA Stuart provides a detailed description of the root: ‘long and woody, pale reddish-brown externally and yellowish internally. It
has a thin bark, a peculiarly disagreeable odor, and a bitterish acrid flavor, leaving a faintly sweet after-taste. It is used in India and Java as a substitute for licorice, but is not employed medicinally by the Chinese. Waring directs an extract to be prepared in the same way as the Extractum Glycyrrhizae of the British Pharmacopoeia’ (Stuart 1911). While the root had been utilised medicinally, some concern has been expressed regarding its potential toxicity (Watt & Breyer-Brandwijk 1962). In India and Africa it was employed for treating gynaecological disorders, although its use to induce abortion does
Extractum Glycyrrhizae (Liquorice Extract) from the British Pharmacopoeia, 1914.
suggest poisonous qualities.11 In Malaysia a root decoction was taken as a cure for colic, and on the Pacific island of Palau the roots provided a remedy for leprosy and arthritis (Perry & Metzger 1981). In Chinese medicine the roots, vine and leaf were decocted for use as an anti-inflammatory and diuretic agent. This could be applied locally for the treatment of tinea infections, scabies, pyoderma (bacterial skin 11 One recommendation noted the use of the fresh fruit decoction taken three times daily to induce abortion (Silja 2008). This sounds potentially dangerous, depending on the heat exposure of the mixture.
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infection) and eczema, as well as being taken for a sore throat or hepatitis. The leaves were also said to be a useful remedy for bronchitis (Hong Kong CMRI 1984b). At least some of these uses appear to be substantiated by studies that have isolated potent antiplatelet, anti-inflammatory and anti-allergic compounds (abruquinones) from Precatory Bean roots. Triterpenoid saponins (and acetate derivatives) with anti-inflammatory attributes were present in the herb (aerial parts). The latter is of interest because the leaves have often been recommended for inflammatory conditions. For instance, a leaf paste (made with oil) was used for treating swellings and rheumatism in India (Anam 2001; Kuo 1995; Wang 1995; Kapoor 1993).
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Chemically Related Toxins
The protein-based toxins of the Precatory Bean (abrin) and the Castor Bean, Ricinus communis (ricin) are very similar in composition. In 1884, initial investigations in Calcutta by the researchers CJH Warden and LA Waddell isolated abrin as the toxic component of the Precatory Bean. A few years later the Castor Bean toxin was isolated and named ricin. In 1891, some insightful original
The Abrin Toxin
The major poisonous compound in the seed of Abrus precatorius is abrin – one of the most toxic chemicals known. One seed contains enough of the toxin to be fatal. Indeed, Professor Len Webb recorded the death of a child at Rockhampton after eating the seed in the 1940s. This is a fairly rare occurrence because the mature seeds, if accidentally swallowed, pass through the gastrointestinal tract intact. They have a very hard seed coat that is impervious to the digestive processes - an extremely fortunate circumstance that has saved many children playing with the strings of ‘pretty beads’. However, the immature green seed coat is soft and easily punctured, making it a more likely candidate for involvement in incidents of poisoning. That said, even skin contact during the process of threading the beads has been linked to incidents of poisoning (Webb 1948). Certainly the Aboriginal practice in the Northern Territory of soaking the seeds to soften them and then drilling a hole with a heated wire rings alarm bells (Wightman 1991; Smith & Wightman 1990). Doubtless the ornamental uses of these ‘bush beads’ occurred in other parts of the country and has possibly been responsible for some unexplained human fatalities.12 The ornamental beads are doubly poisonous when worn due to the skin contact. As babies and young children tend to chew on such attractive items, this could have easily resulted in deaths. However, it is also possible that piercing the bean and prolonged boiling would have had enough of a detoxicant effect to neutralise the danger.
Abrus precatorius vine with seeds.
research as to their mechanism of toxicity was undertaken by Paul Erlich, who did studies on animal immunisation with subcutaneous injections of very small doses of abrin and ricin. He found that immunity was specific to each toxin and not interchangeable. Therefore immunisation with ricin would not work for abrin-poisoning and vice versa. Interestingly, the immunity was transferable from the mother, via her blood in utero and during lactation. His studies were ingenious in that they determined both toxins were composed of two separate parts (a binding agent and a toxin) with a different chemical construction. Interest in the subject later waned and it was not until the early 1970s that JY Lin and colleagues were to confirm his proposition and expand on the chemistry of these unique toxins (Olsnes 2004). 12 I have personally seen these beads advertised for making jewellery in northern Queensland. Once, about ten years ago, in a shop in England I found ornamental Precatory seeds strung on string for use as beads. Both incidents prompted an immediate warning of the danger.
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Similar to the Castor Bean, the seeds of the Purging or Physic Nut (Jatropha curcas) are oilrich (up to 55%) – although they contain a toxin, curcin (jatrophin), with chemical properties equivalent to that of abrin. After detoxification the oil is suitable for making candles and soaps, as lighting fluid, and for lubrication purposes.
Jatropha curcas seeds. (Courtesy: Frank Vincentz, GFDL, Wikipedia)
Despite the fact that the toxic component is not as potent as abrin, the gastrointestinal effects can be equally drastic. Roasting the nut may not completely eliminate its toxicity and therefore the pomace (the residue after oil extraction) can retain purgative attributes. The oil was once widely recommended as a purge for constipation, intestinal parasites, and intestinal pain – although its effects were so drastic it was known by the descriptive name ‘Hell Oil’. The toxic effects were very similar to those of Castor Oil (beans) and Precatory Bean (seeds) – violent gastric irritation, dehydration and collapse. Accidental poisoning of children was frequently reported, albeit recovery was usually relatively quick (Morton 1977; AbduAguye 1986; Joubert 1984).
A Potent Reputation against Evil
The records of Chinese traditional medicine show great familiarity with the poisonous properties of the Precatory Bean. The Reverend GA Stuart,
Croton tiglium, from Koehler’s Medicinal Plants, 1887. Croton tiglium, known as the ‘Purging Croton’, has effects similar to that of the Castor Oil bean and the Purging Nut.
in his Chinese Materia Medica: Vegetable Kingdom (1911) noted that Abrus seeds could ‘permeate the nine cavities of the body [and] expel every sort of evil effluvia from heart and abdomen’. The description of these potent effects agrees very closely with its toxicity. In Chinese traditions the seeds were attributed with potent protective magical properties that were extremely useful for repelling evil ‘devils’ – a reputation shared by Ricinus communis and Croton tiglium. Indeed, in the case of a ‘catdevil’ attack, the ancient medical text, the Pent’sao, recommended that pills be prepared from a bean of each plant pulverised with cinnabar and wax, and taken immediately: ‘Then surround the patient with ashes and place before him a cinder fire. Spit the medicine into the fire, and as it bubbles up, mark a cross on the surface of the fire, when the cat-devil will die.’ With reference to Croton tiglium Stuart also comments: ‘The drug is recommended for a very large number of difficulties, but, generally,
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speaking, the Chinese doctors are afraid to employ it on account of the exaggerated notion of its poisonous properties, which were handed down from very ancient times’. Its medicinal uses included colds and fevers, throat problems, gastrointestinal distress (obstinate diarrhoea, dysentery), delayed menses, neurological problems (paralysis, apoplexy), and externally for diverse skin disorders. The seeds, coarsely powdered, were also recommended to treat various forms of drug poisoning. In India the use of minute doses of abrin in animals has been known to induce a level of immunity to the toxin. Later, anti-abrin and anti-ricin serums were developed – although their effectiveness has been greatly debated. An awareness of this potential led to its practical use by criminals as an antidote to ordeal poison. As GL Robb observed: ‘the greatest drawback [to its use as an ordeal poison] was that immunity could be established by the repeated ingestion of small doses. This last factor is undoubtedly the reason for its somewhat restricted use even as an accessory poison’. For non-immunised persons unfortunate enough to have been sentenced to trial by ordeal, the results were dramatic: ‘The accused underwent severe vomiting, purging, general weakness, an inability to stand up, cold perspiration, colic, depressed and then accelerated heartbeat, trembling, and finally, heart failure’ (Robb 1957). Obviously, if they died they were guilty of the crimes for which they were accused – and the community was better off without their participation. Accidental poisoning is associated with similar symptoms that generally appear 2–3 hours after taking the toxin, although the time lapse can be longer, extending from several hours to 1–2 days. In addition to severe vomiting there is a tendency to haemorrhage. This usually involves the retina of the eye and bleeding of the small intestine, with associated tissue necrosis (cell death). Substantial fluid loss occurs, resulting in shock. There are no specific antidotes, and therefore treatment is symptomatic (Iwu 1993; Frohne & Pfander 1984; Watt & Breyer-Brandwijk 1962). Even so, the Chinese Medicinal Herbs of Hong Kong
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(1984b) makes note of a herbal antidote prepared from a decoction of Chinese Liquorice (Glycyrrhiza uralensis 10 g) and Honeysuckle (Lonicera japonica 12 g). Unfortunately, comments regarding its efficacy were not recorded. Indian Ayurvedic traditions also hold that a mixture of Amaranthus juice and sugar has antidotal properties (Vaidya 2005).
The Fine Line Between Toxin and Therapy
It is no surprise to find records regarding the use of the Precatory Bean as a deliberate toxin. In Southeast Asia a powdered seed paste was employed as a dart and arrow poison. Wounds were generally said to be fatal within 24 hours. In addition to its direct toxic effects, injected abrin has a very powerful irritant activity that produces localised oedema and ecchymosis (bruising). However, heated infusions have substantially reduced irritant potential and, if taken orally, the preparation appears to be further inactivated by the digestive process. Complete detoxification is possible – although this occurs only if the seed is very carefully prepared.
The type of processing employed could explain some of the more unexpected medicinal uses of this plant. The seed paste was recommended in Chinese medicine for tinea infections, scabies, pyoderma and eczema. The remedy was also noted to have diaphoretic, expectorant and antiperiodic attributes (Hong Kong CMRI 1984b). In Indian medicine the seed paste was used as a rubefacient for treating sciatica, stiff shoulders, paralysis, and other neurological problems13 – as well as for skin diseases, ulcers and inflammations (Kapoor 1993). In Cambodia the seeds have been incorporated into a compound antimalarial prescription that was prepared as a decoction (subjected to prolonged boiling) which probably destroyed the abrin (Burkill 1935). However, any incautious use can quickly result in poisoning. Its use, even externally, must therefore be viewed as fraught with potential for disaster. In the past, the Precatory Bean was used for the 13 Abrus precatorius and A. schimperiana leaves have been used as a tea or decoction for treating epilepsy in Tanzania. Investigations have shown extracts possessed anticonvulsant and CNS depressant activity (Moshi 2005; Adesina 1982).
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Abrus vine in rainforest canopy.
treatment of ophthalmic disorders – although the remedy has little to recommend it. The use of the seed infusion as eye drops for the treatment of conjunctivitis has resulted in fatal poisoning due to the absorption of abrin through the conjunctiva. Other side-effects have included severe conjunctivitis, permanent opacity (cloudiness) of the cornea, and blindness. Scarily, even ‘complete destruction of the eye’ has occurred. Henry Burkill (1935) noted: ‘A powder of the decorticated seed, or an extract made from it, placed in the eye causes inflammation which European ophthalmic surgeons have made use of for clearing away opacities of the cornea. The practice commenced in 1888, but has not found favour, being too drastic. The chemical substance abrin causes the inflammation; Ricin from castor oil seed has similar but milder action and is preferred.14 Outbreaks in jails of inflammation of eye
have been traced to Abrus seeds, used for the purpose of malingering.’ The latter seems to border on sheer stupidity. The use of the leaf vapour (leaves crushed and boiled in water) as a remedy for eye inflammation would appear to be a safer option. Indeed, in Cambodia the leaf juice was used for the treatment of conjunctivitis. Although its toxic reputation would tend to advise caution in its use, the use of the Precatory Bean as an antiparasitic agent appears to have been quite widespread. Chinese medicine recognised that the Precatory Bean seeds were capable of destroying ‘every sort of visceral or cuticular worm’ (Stuart 1911). A traditional Indian antiparasitic mixture that incorporated the Precatory Bean (seed) also contained Onion (Allium cepa), Allium sativa, Lemon (Citrus limon) and Turmeric (Curcuma longa), blended in sesame oil. Studies have confirmed its effectiveness. The paste was applied daily to pigs with scabies infestations and the problem was completely eliminated within six days, without any later recurrence (Dwivedi & Sharma 1985). In Africa, Abrus precatorius has been used as an emetic and purgative, and for treating bilharziasis, intestinal parasites (including tapeworm) and other forms of gastrointestinal distress. It is, however, important to know which part of the plant was utilised, the preparation process and method of application. A large Zimbabwean study of traditional treatments for schistosomiasis interviewed 286 traditional healers and identified various plant extracts, including Abrus precatorius, which were effective against the parasite. Later studies confirmed the anti-schistosomial activity of the Precatory Bean vine (stem and root).15 It was also effective against tapeworms (Ndamba 1994; Molgaard 2001). In some traditions Abrus precatorius roots and seeds have been used as gastrointestinal remedies. They were reported to have anti-diarrhoeic properties, while the bark had an anti-dysenteric activity. Experimentally, a seed extract has shown an antispasmodic effect on the intestinal musculature – which supports its use for treating diarrhoea and stomach pain (gastralgia) (Iwu 1993; Nwodo 1991; 14 The safety of ricin would be equally doubtful. 15 Other plants that were active against the schistosoma parasite included Pterocarpus angolensis, Ozoroa insignis (bark, leaves), Zizyphus mucronata (root-bark) and Elephantorrhiza goetzei (stem bark) (Molgaard 2001; Ndamba 1994).
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Oliver-Bever 1986; Wambebe & Amosun 1984). In African traditions an Abrus seed-based remedy has been used to treat urinary disorders and venereal disease (notably gonorrhoea). Studies of seed extracts tend to confirm its efficacy in this regard, particularly its antispasmodic and antimicrobial properties. Extracts were very active against Staphylococcus aureus and Escherichia coli – although stem and seed oil were also active against some additional grampositive bacteria and Candida albicans (Adelowotan 2008; Watt & Breyer-Brandwijk 1962). Compounds (isoflavanquinones) have been isolated from the plant (aerial parts) with antitubercular and antiviral activity – as well as antiplasmodial and cytotoxic properties (Limmatvapirat 2004). This readily attests to the complex chemistry of the plant. These findings support the use Abrus precatorius as a remedy for asthma, chest pain, and infection (including bronchitis and tuberculosis), colds, coughs and influenza. More dubious recommendations have included the use of the seeds as an aphrodisiac in India and Africa – although an Arab recipe, which boiled the seeds in milk, possibly subjected them to enough heat to inactivate the toxin (Watt & BreyerBrandwijk 1962). The seeds have also shown definite anti-fertility properties. Extracts have induced sterility in male animals – notably the inhibition of sperm production, as well as an anti-motility effect on sperm (Ratnasooriya 1991; Sinha 1990; Sinha & Mathur 1990; Rao 1987; Sharma & Verma 1987; Jadon & Mathur 1981). The use of the leaf as a sexual tonic appears to be a decidedly safer alternative. The leaf powder, mixed with honey, has been taken to treat impotence in Cameroon (Noumi 1998). Commercially, the physical characteristics of the oil make it useful as a lubricant for machinery, as a hydraulic fluid, and it is even suitable for use in diesel motors. The oil will not solidify in extreme cold and will retain its viscosity at high temperatures, making it eminently suitable for use in aircraft and locomotive engines. Numerous gynaecological and obstetric remedies have employed the Precatory Bean. Its uterine tonic, oxytocic, abortifacient and anti-fertility effects have been verified experimentally (Vedathy 1995; Nwodo 1991; Sethi 1990; Oliver-Bever 1986; Nwodo & Botting 1983; Zia-ul-Haque 1983). Central African
A Toxic Aphrodisiac
White Abrus seeds. (Courtesy: RameshRaju, Wikipedia)
The classic symptoms of Abrus poisoning involve gastrointestinal distress (abdominal pain, bloody diarrhoea), central nervous system dysfunction (encephalitis, sensory problems, confusion, seizures), coma, and renal failure leading Abrus precatorius seed. to death. There are a couple of uncommon colour forms of the Precatory Bean – black seeds with a white spot, and vice versa. No matter their colour, all Precatory Bean seeds are dangerously toxic. It could be quite easy to confuse the black and white seed forms with some edible seeds. One report of poisoning by a white-seed variety, which was recommended as a highly hazardous aphrodisiac, mentioned that the person involved took ‘several’ seeds – although two or three are regarded as being a fatal dose. This resulted in prolonged hospitalisation and treatment with antimicrobials, anticonvulsants and supportive therapy. He survived (Pillay 2005). There are also reports of suicide attempts that have employed the extracted seed powder, some of which were fatal, while others have recovered with hospitalisation (Reedman 2008; Sahoo 2008; Subrahmanyan 2008).
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tribes utilised the powdered seed as an oral contraceptive and one dose was reputed to be effective for more than a year (Iwu 1993; Watt & Breyer-Brandwijk 1962; Quisumbing 1951). In India it enjoyed a similar reputation as an effective contraceptive, as well as being useful for regulating menstrual problems (i.e. emmenagogue activity). Root extracts have effective anti-oestrogenic properties, while the seed extract was an abortifacient. A steroidal fraction of the seed oil was shown to produce sterility in animals (Satyavati 1976). In India and Africa preparations of the seed and roots have also been used to procure abortion, and to facilitate labour. Extracts of the seeds, roots and the plant juice were used locally (vaginally) as an abortive. Henry Burkill suggested that the use of the roots was less dangerous than seed preparations: ‘It may be suggested that … the roots are used [because] the fear of consequences of abortion … [using] the crushed seeds has dictated a trial with a milder part of the plant.’ The leaf powder, which was mixed with cow’s milk and sugar, has also provided a remedy for leucorrhoea (vaginal discharge) in India (Vijayakuman & Pullian 1998).
The Castor Oil bean, which contains the abrin-like toxin ricin, has been effectively used as an antifertility agent. In many Southeast Asian countries, as well as India, Algiers, Africa and Egypt, the seeds were employed as a contraceptive – in a diverse array of preparations. In Algiers the beans were dipped in the warm blood of a rabbit before being taken. Egyptian women claimed that taking one seed after the birth of a child would prevent pregnancy for at least nine months. There seems to be some truth to these claims, as animal testing demonstrated an 80 per cent inhibition of pregnancy, which was reversible (Salhab 1997; Al-Tahan 1994). Still, this use of the seed must be regarded as courting danger. (Image courtesy: Kim and Forest Starr, Hawaii)
A New Order of Anticancer Drugs?
The Precatory Bean has had a long history of use as an anticancer herb. Between 1852 and 1935 the seeds were repeatedly mentioned in treatments for skin and mucous membrane cancers, including epithelial cancer of the hand, skin and other mucosal surfaces – the powdered seed was directly applied to the lesion. In the early twentieth century (1907) Rampoldi mentioned that the use of jequiritin (probably referring to abrin or a form of seed extract) had produced remission of skin carcinomas in 100 patients.16 Precatory Bean extracts have shown potent cytotoxic activity, leading to investigations of its anticancer potential, which have focused on abrin (Ramnath 2002b; Iwu 1993; Minyi 1992; Oliver-Bever 1986). Castor Oil seeds, which have toxic properties comparable to abrin, have shown similar anticancer effects (suppression of tumour growth) and anti-leukaemic activity. Abrin and ricin are thought to act by inhibiting protein synthesis in cancer cells, thereby inducing programmed cell death (apoptosis) (Ramnath 2009; Hasegawa 2000; Ohba 1997; Iwu 1993; Hegde & Podder 1992; Kanellos 1990; Lin 1978; Morton 1977; Closs 1975; OliverBever 1971). There has been substantial research into the mechanisms by which this occurs, with recent investigations showing immunostimulatory properties for Abrus lectins that appear to have an influence on its anticancer potential (Bhutia 2009a, 2009b, 2009c, 2008; Ghosh 2009; Ghosh & Maiti 2007a, 2007b; Ramnath 2006; Tripathi & Maiti 2005, 2003). Evaluations of the seed powder have also shown a good flavonoid and phenol content, with extracts demonstrating significant antioxidant activity (Pal 2009). The toxic lectins in Abrus are similar to a number of highly problematic bacterial toxins – those from diphtheria, Pseudomonas, cholera, anthrax, and the Shiga toxins from Shigella dysenteriae. They have two functionally different parts: a receptor-binding agent and an enzymatically active component (Olsnes 2004). Lectins are particularly useful for biochemical investigations. For example, lectins from Abrus precatorius have helped to identify some of the cellular functions that are involved in Alzheimer’s disease 16 Rampoldi R. Annali di Ottalmologia, 1907, p. 206. Mentioned in Casey A Wood. A System of Ophthalmic Therapeutics Being a Complete Work on the Non-Operative Treatment, Including the Prophylaxis, of Diseases of the Eye. Cleveland Press, Chicago, 1911.
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(Zambenedetti 1998). Other lectins of similar interest include modeccin from the South African plant Modecca (Adenia digitata, syn. Modecca digitata), volkensin (from Adenia volkensii), and viscumins from Mistletoe (Viscum album) (Olsnes 2004). Lectins may be suitable for use in drug-delivery protocols aimed at specific target cells. Anticancer drugs named ‘immunotoxins’ have been developed from these lectins that can be used in combination with other substances. By means of a specialised biochemical delivery system, they insert anti-cancer drugs into a cancer cell (Olsnes 2004). Cells with specific receptors are therefore targeted by the delivery of a toxin that is designed to induce cancer cell death. Equally useful toxins have been sourced from other herbal resources – that is, Pokeweed antiviral protein (Phytolacca decandra), saporin (Saponaria officinalis) and gelonin (Gelonium multiflorum seed). Bacterial toxins such as Pseudomonas exotoxin and the diphtheria toxin have similar potential (Pastan & Kreitman 1998; Draper 1978). A ricin-based immunotoxin treatment has undergone clinical trials in Hodgkin’s and nonHodgkin’s lymphoma patients, in combination with other therapies, and the results have been rated as moderate to good17 (Longo 2000; Schnell 2000; Vose 1999). There is the possibility that future drugdelivery systems utilising immunotoxins could be developed for the treatment of drug-resistant forms of malaria and chronic inflammatory disorders (Surolia 2000; Thepen 2000).
Murder and Mayhem: The Toxic Castor Oil Plant The Castor Oil plant (Ricinus communis) has an ancient history. It is native to the Mediterranean, eastern Africa and India. Evidence of its use has been found in Egyptian tombs dated around 4000 BC, where the seeds provided a slow-burning lamp oil – and somewhere around 600–900 AD the herb was introduced into China. The attractive-looking
17 Abrin has shown immunopotentiating properties in non-toxic doses. Ricin from the Castor Oil bean (Ricinus communis) has likewise shown immune stimulatory and anti-inflammatory activity (Ramnath 2002a).
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In Australia the Castor Oil plant has been declared a noxious weed. It has an opportunistic growth habit that allows it to easily displace desirable native species, particularly in riverine and woodland areas. Originally the plant was native to Africa and Asia, although it is now found across the globe, often in ornamental cultivation. The seeds are easily spread by machine and water, and germinate readily. Throughout the Australian continent the shrub has has self-propagated, spreading to form dense colonies. In many outback regions these have turned into an impenetrable pest that has seriously reduced the availability of grazing lands (Smith 1995). (Upper Image courtesy: The Tannykid, flickr) seeds have a deadly potential which unfortunately is enhanced by their hazelnut flavour – which does not, therefore deter experimentation. A single seed can be lethal to an adult (dose: 0.25 g of toxin), although some individuals have ingested more and survived. The method of detoxifying the seed oil by heat was a truly amazing discovery – albeit likely to have been
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Castor Oil seeds have a rather attractive mottled appearance and a very hard seed coat. Their toxic potential is similar to that of the Precatory Bean. In the past children playing with the ‘beads’ or seed necklaces have become the unwitting victims of poisoning. More disturbing has been the deliberate use of seed extracts for homicide. In Africa, the crushed seeds were added to food as a means of infanticide. Malingerers have even applied it to the conjunctiva of the eye to incite inflammation – an extremely dangerous practice. (Image courtesy: USDA, Agricultural Research Service)
Fatal doses (in adults) range from 2–20 seeds, depending on whether the seed coat is breached. Crushing the seed rapidly releases the toxin. Animals are equally susceptible to poisoning, and as few as six seeds can kill a horse. Torald Sollmann noted: The ricin is responsible for the toxic effects on eating the castor seeds; five or six of these are fatal to a child, twenty to adults; three or four seeds may cause violent gastroenteritis, with nausea, headache, persistent vomiting, colic, sometimes bloody diarrhoea, thirst, emaciation and great debility. The symptoms usually do not set in until after several days. More severe intoxications cause small frequent pulse, cold sweat, icterus and convulsions. Death occurs in six to eight days, from the convulsions or from exhaustion. The fatality is about 6 per cent. This low fatality is due to the destruction of the poison in the alimentary canal (Sollmann 1949).
This intestinal detoxification process appears to have allowed some to survive the unhappy effects of poisoning. In acute cases the symptoms can take from 2–24 hours to appear, although occasionally they have been delayed as long as three days. The accessory symptoms of poisoning can be equally distressing: chills, fevered hot skin, blurred vision, lethargy, drowsiness, cyanosis, convulsions, circulatory collapse, and possible kidney failure. The fact that ricin has blood-coagulant
properties similar to abrin is another dangerous consideration in incidents of poisoning. The effects can be widespread in the body, causing severe necrosis (cell death) in the liver, spleen and lymphatic tissue (Morton 1977). However, individual reactions are influenced by a couple of factors. Firstly, ricin has great stability in the digestive tract, so a large amount can be absorbed without having an immediate toxic reaction, hence the variable delay in manifestation of symptoms. Secondly, if the kernels have not been chewed the amount of toxin released is substantially reduced and the chances of survival dramatically improved. Modern medical management of poisoning incidents has made enormous advances in treatment, making fatalities highly unlikely (Doan 2004; Morton 1977). Even so, many domestic animals and poultry have died from eating Castor beans that have been inadvertently mixed with their feed, or being fed unprocessed presscake following oil extraction. Cattle appear less susceptible, although large doses will inevitably have toxic results (Morton 1977).
Biowarfare Agents
Castor oil has a rather unsavoury history as an instrument of interrogation and torture. In Fascist Italy, during Benito Mussolini’s reign, excessive doses were used to purge dissidents. This would have been humiliating in the extreme – and lead Castor Oil plant. to subsequent lifethreatening dehydration. The beatings by the Blackshirt interrogators would have seriously complicated the chances of survival, and those who did survive would have suffered from permanent colonic damage. However, the Castor bean has substantially more toxic potential. The original investigations into the development of ricin as a biological
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warfare agent were initiated in World War I by the US Chemical Warfare Service. The British took it a step further with the development of a ricin bomb (W-bomb) in World War II. Fortunately, it was never used. Meanwhile, some Eastern European countries developed deadly weapons that utilised ricin. When injected, the toxin is 100 times more potent than would be expected with oral exposure (Olsnes 2004). In September 1978, the drug achieved a disturbing level of notoriety when it was thrust into the international spotlight by a Cold War espionage incident in London. This involved the assassination of Georgi Markov, an exiled Bulgarian playwright and novelist, who was critical of the decadent behaviour of the communist leadership in his country. The secret police appeared to be equally unimpressed with his criticism. Opinion generally concurred that his abrupt demise was no accident. Mrs Markov mentioned that, as her husband waited for a bus, he felt a jab in his thigh. He saw a man drop an umbrella – who then apologised and caught a taxi. A few hours later Markov became very sick and feverish, and three days later he died in St James’s Hospital. At autopsy a tiny, pin-sized (1.52 mm) metallic sphere was found in a puncture wound. It had two minute holes bored through it, which allowed the release of the toxin (around 200– 250 mcg). At the time of his death this minuscule amount was no longer detectable, yet his symptoms all pointed to ricin poisoning (Olsnes 2004; Frohne & Pfander 1984). The re-examination of a poisoning incident involving Vladimir Kostov, another Bulgarian, at a Paris metro station, led to the discovery of a platinum ‘bullet’ containing ricin. Kostov became acutely ill, but was saved because the ricin did not dissolve quickly enough before becoming embedded in fatty tissue, thereby limiting its release. Five similar cases were uncovered, and it is likely there have been others. Fortunately, although there are rumours of ricin being associated with other terrorist groups, it is now much easier to detect the toxin in the body. The availability of a vaccine has further limited its usefulness as a deliberate poison (Olsnes 2004).
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However, vaccines and prophylactic strategies are only useful against injectable forms of the toxin when given a few hours after exposure – they are ineffective against aerosol formulations (Doan 2004). The reputation of ricin as a toxin has not abated, however. Ricin has been found in American postal facilities (South Carolina, the White House) and a US Senator’s office – obviously planted with sinister intent (Audi 2005). There is also a recent report of a Belgian man deliberately using a castor oil injection for suicide. He was conscious on admission to hospital having experienced nausea, vomiting, diarrhoea, dyspnoea, vertigo and muscular pain. Despite treatment he died nine hours later due to multiple organ failure (Coopman 2009).
Image of envelope in which the letter containing anthrax was sent to Senator Tom Daschle during the 2001 anthrax attacks. (Permission: PD-USGOVFBI. Wikipedia)
Toxins that are bioavailable by an inhalational route have been the most favoured for biowarfare purposes. Currently, the most potent toxin weapon candidates continue to include ricin, botulinum toxin (Clostridium botulinum), staphylococcal enterotoxin B (produced by Staphylococcus aureus), saxitoxin (a marine dinoflagellate toxin) and fungal mycotoxins (trichothecenes, mainly from the Fusarium genus). There is also anthrax (Bacillus anthracis), although this is difficult to obtain. In the 2001 anthrax attacks in the United States twenty-two people contracted the disease. Of these, eleven progressed to develop a life-threatening condition, with five of them
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dying from inhalational anthrax. Anthrax, along with botulinum toxin and aflatoxin, were among the biological weapons that were produced by Iraq during the 1990s. Aerial bombs containing these toxins were manufactured, as well as spraying devices for helicopters and unmanned aerial vehicles (Pita 2009).
A Problematic Allergen
The flowering spike of the Castor oil plant has both female and male flowers. At the top female flowers produce seed heads, while male flowers on the lower portion wither and die after pollination occurs.
storage. Those who are sensitive to this substance can suffer severely from contact with any part of the plant – and even contact with the broken seed can cause life-threatening allergic reactions. Workers in factories dealing with Castor oil have reported various degrees of respiratory, cutaneous and digestive disorders. Discomforting reactions can even result from atmospheric exposure to the plant in communities living near processing plants. Gardeners have experienced dermatitis from merely handling the Castor pomace (Morton 1977).
Pollen from Castor Oil plant. (Courtesy Dartmouth E.M. Facility, Dartmouth College, Hanover, NH, USA)
Castor Oil: from Household Purge to Commercial Lubricant
In addition to ricin, Castor oil seeds contain the less toxic alkaloid ricinine, an enzyme (lipase), and a highly potent allergen (CBA). The latter compound is not destroyed by heat and will survive prolonged
The regular use of Castor Oil has, thankfully, passed into obscurity – although it was once regarded as an indispensable, albeit unpopular, component of the medicine cabinet. Almost seventy years ago a comprehensive review by the herbalist Maude Grieve offered a good insight into its prior importance: Castor Oil is regarded as one of the most valuable laxatives in medicine. It is of special service in temporary constipation and wherever a mild action is essential, and is extremely useful for children and the aged. It is used in cases of colic and acute diarrhoea due to slow digestion, but must not be employed in cases of chronic constipation, which it only aggravates whilst relieving the symptoms. It acts in about five hours, affecting the entire length of the bowel, but not increasing the flow of
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Antique Castor Oil bottle. (Courtesy James Ross, www.goldengateantiques. com)
The British Pharmaceutical Codex of 1949 lists the ‘Action and Uses of Oleum Ricini (Castor Oil)’ as:
Castor Oil, from Peter Squires’ Companion to the latest edition of the British Pharmacopoeia, comparing the strength of its various preparations with those of the United States, and other Foreign Pharmacopoeias, to which are added Not Official Preparations and Practical Hints on Prescribing, London, 1899. bile, except in vary large doses … The oil will purge when rubbed into the skin, or injected. It is also used for expelling worms, after other special remedies have been administered (Grieve 1931).
The repulsive taste of this common household remedy was a substantial deterrent to its use. In the intestine the oil undergoes a chemical change (under the influence of pancreatic enzymes) that gives it a mildly irritant action leading to a ‘loosening of the stools’ within a few hours. Hence Castor Oil’s reputation as a colonic cleansing agent – although this irritant tendency made it unsuitable for use during menstruation and pregnancy, or in individuals with irritable bowel disorders. Its detrimental potential should not be underestimated. In the past the oil was even used to initiate labour, as irritation of the intestinal tract caused a reflex stimulation of the uterine muscle. Its administration can be downright dangerous in cases of intestinal obstruction and appendicitis. Castor Oil continues to be used medically for treating cases of food poisoning, and to ‘clean out’ the intestine before investigative examinations.
a mild purgative, its action being exerted as a result of saponification in the small intestine, with formation of the irritant alkali ricinoleate. The laxative action of castor oil takes effect in from four to eight hours and occasions little or no griping. It is used in the treatment of haemorrhoids or during pregnancy and is useful for emptying the bowel in diarrhoea due to food poisoning. Small repeated doses of 0.3 to 0.6 millilitres (5 to 10 minims) may be given in the intestinal colic of children. The oil is sometimes used with olive oil, as a rectal injection to remove impacted faeces. Externally, castor oil is sometimes applied, generally mixed with other emollients, for bed sores. Zinc and castor oil cream is used as an emollient and astringent, particularly for infants. Castor oil is often used as an ingredient of spirituous hair lotions. It is a soothing application when dropped into the eye after removal of foreign bodies, and is an excellent solvent for alkaloids, such as cocaine and atropine, for application to the conjunctiva. Castor oil is best administered in milk or lemon juice, or in capsules. The dose would be administered an hour before breakfast, on an empty stomach.
Castor Oil when freshly extracted is relatively odourless, with a mild flavour and an equally mild laxative effect. However, as it ages and becomes more rancid (oxidised), the purgative effect becomes more noticeable. The seeds must be stored unbroken or they, too, quickly become rancid – with the subsequent development of a characteristic nauseating taste. To produce high-grade medicinal oil the seed coat is removed and the kernels are immediately coldpressed. The oil then requires refining, which removes the albumin and enzyme traces, thereby enhancing its keeping quality. This oil has been of great practical value
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for pharmaceutical preparations such as contraceptive jellies, foams and creams, and in eye medications as a soothing and cleansing agent. A lower grade oil can be procured from a second pressing. Oils used for industrial purposes do not need the seed coat removed before processing because they are exposed to higher temperatures and additional processing methods to increase the yield – and adequately detoxify the product in the process. Castor oil has other diverse practical attributes that have made it indispensable in many industrial processes (Morton 1977): • I t is a source of sebacic acid, which is used for making nylon and other synthetic fabrics, including linoleum, artificial leather and rubberlike foam products – as well as typewriter ink, fly-paper, candles, hair oils and cosmetics. • The seeds yield lipase, a substance which is used to make soap transparent and improves its lathering capacity in cold water. • Commercially, Castor oil can assist in the process of producing glycerine and free fatty acids from vegetable oils, thereby allowing glycerine extraction. A dehydrated form of the oil is extremely useful as an additive to paints, enamels and varnishes. • Castor oil, under the name Turkey Red Oil, has been used in dyeing and printing processes, serving as a dye fixative and for ‘dressing’ leather goods. • The seed residue remaining after extraction of the oil – i.e. the ‘castor pomace’, has been utilised as a soil fertiliser. However, only when it is subjected to heat processing can this seedcake be used as animal feed. • The oil has good burning properties and has been used as an illuminant. Indeed, the seeds have been threaded onto wooden splinters in South America to provide a crude form of candlelight.
A Popular Remedy for Skin Disorders
Castor oil has been widely utilised as an emollient antiirritant for treating itching (pruritic) skin problems such as ringworm, tinea and nappy rash. The oil has soothing properties and has been used as a protective agent to prevent the discomfort associated with contact allergens. The Castor Oil plant (particularly the leaf ) has long been a popular antibacterial folk medicine. In Australia, Aboriginal people used the leaf-lotion for treating ringworm infections. This was left on the skin for a couple of days, and then the area rubbed with a leaf of the Sandpaper Fig to remove the affected skin (Drewes 1991). In Africa the crushed leaves provided a dressing for burns, ulcers and sores – in particular, the hot poultice was recommended for guinea-worm sores. In addition to its antifungal properties, it has effective antibacterial actions against a range of microorganisms, including Mycobacterium tuberculosis (Iwu 1993; Oliver-Bever 1986; Watt & Breyer-Brandwijk 1962). The antifungal fatty acid, undecylenic acid, is produced by vacuum distillation of castor oil. This is the main active ingredient in many over-the-counter topical antifungal remedies. It is also effective for the treatment of intestinal, oral and vaginal candidiasis (Altern Med Rev 2002). Just about every part of the herb has been utilised therapeutically in diverse medical traditions. The fresh leaves have been applied to the abdomen to treat ‘internal complaints’, while the heated oil was useful to ease the pain of rheumatic joints, swellings and inflamed muscles. A leaf infusion has been used as an eye wash, while root decoctions were taken as remedies for lumbago, sciatica and related ailments.18 However, the root-bark is reputed to have drastic purgative properties (and was probably removed in many instances) that would have made it a decidedly unpleasant medicament. Such considerations did not prevent its use as a remedy for ‘gripe’ in horses. In veterinary practice, castor oil has been regarded as an exceptionally effective external emollient that was widely used for treating skin diseases and wounds. Less appealing was the use of a remedy composed of the oil mixed with turpentine to expel tapeworms. The leaves 18 Recent investigations have supported the safety of root extracts for medicinal use (Ilavarasan 2011).
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were reputed to have insecticidal properties, which led to the herb commonly being cultivated around houses in Egypt and South America. Castor oil has even been
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added to leftover food scraps as a cockroach poison (Iwu 1993; Drewes 1991; Morton 1977; Watt & Breyer-Brandwijk 1962).
Table 8.3 Modern investigations into the Castor Oil plant
This table is limited to plant extracts and their active components, and does not include recent research on ricin or the extracted oil. Properties Antibacterial
Research details Seed extract (fermented extract of de-shelled seeds): methanol and water extracts had good activity against Klebsiella pneumoniae, Escherichia coli, Proteus vulgaris and Staphylococcus aureus. Pseudomonas aeruginosa was less susceptible, while Enterococcus faecalis was resistant (Jombo & Enenebeaku 2008). Seed protein extracts: good activity against Staphylococcus aureus (Salahudin 2011). Root extract: good range of antimicrobial activity; hexane extracts had prominent antimicrobial activity against Candida albicans and Aspergillus niger fungal strains. Methanol extracts were active against Escherichia coli and A.niger. Water extracts were inactive (Verma 2011). Leaf extracts: very good antimicrobial comparable to gentamicin against gram positive bacteria (Staphylococcus aureus, Bacillus subtilis) and gram-negative bacteria (Pseudomonas aeruginosa, Escherichia coli and Proteus vulgaris (Kota & Manthri 2011). Oil paste: antimicrobial activity against oral pathogens with potential for use in dentistry (Garcia 2009). Seed extracts: good antimicrobial activity against oral pathogens from immune compromised patients being treated for cancer (Panghal 2011). Leaf extracts: significant antibacterial activity against Escherichia coli, Staphylococcus aureus, Klebsiella pneumoneae, Streptococcus pyogens (Islam 2010). Leaf extracts: antifungal activity against Candida albicans, C. glabrata and C. tropicalis (Jain & Nafis 2011).
Anti-inflammatory and analgesic
Leaf extracts: antibacterial activity against Vibrio spp. with potential for use in aquaculture (Sankar 2010). Studies have indicated herb extracts had anti-inflammatory properties, although it was devoid of an analgesic action (Banerjee 1991). Significant anti-inflammatory and antihistamine activity shown by ethanolic root extracts (Lomash 2010; Ilavarasen 2006). Flavonoids, tannins, alkaloids present in plant extract (Ilavarasen 2006). Experimentally, injections of ricin are highly inflammatory. However, they were shown to influence the release of corticosteroids from the adrenal glands. This effect can therefore reduce the inflammatory activity of other agents and may even be useful medicinally (Morton 1977). Methanol seed extract: fraction has shown antinociceptive activity, possibly linked to oestrogenic action (Okwuasaba 1991).
Anticancer
Antidiabetic
Seed extracts: potent antioxidant activity (Williamson 2002). Leaf extracts have shown cytotoxic properties against various human tumour cell lines, including inducing apoptosis in melanoma cells. Leaf extracts contain 1,8-cineole, camphor, alpha-pinene and beta-caryophyllene as active components (Darmanian 2009). Seed extracts: antitumour activity (Amara 2008). Root extract: significant antihyperglycaemic activity (Shokeen 2008; Dhar 1968).
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Antifertility
Fertility: clinical abortifacient effects can occur from the oil and long-term contraceptive activity from seed extracts (Williamson 2002). A protein isolated from root extracts affects testosterone levels and reduces spermatogenesis (Nithya 2011; Rajo 2006).
Liver and kidney function
Seed extract: anti-implantation and abortifacient effects in animal studies. Oestrogen-like activity (Makonnen 1999; Salhab 1999; Okwuasaba 1991). Leaf extracts have shown significant have liver protective (hepatoprotective) activity. Extracts acted to restore normal liver enzyme function, and had significant choleretic and anti-cholestatic activity. The two main compounds responsible were identified as ricinine and n-demethyl-ricinine (Sabina 2009; Joshi 2004; Kalaiselvi 2003; Zakaria & Mohd 1994; Visen 1992; Tripathi 1991).
Nervous system activity
Seed (ethanol) and leaf (aqueous) extracts: diuretic effect in animals (Williamson 2002). Pericarp extract from seed: central nervous stimulant activity. Low doses had neuroleptic activity in animal studies. Ricinine showed memory improving effect and seizure-eliciting properties (Ferraz 1999).
Antiparasitic
Fresh root extract: protective effect against convulsions (Williamson 2002). Antiparasitic activity: antiamoebic against Entamoeba histolytica (water and ethanol root and stem extracts); anti-schistosomal activity against Schistosoma mansonii (seed oil); antifilarial and nematocidal (leaf extracts) (Williamson 2002). Extracts have shown activity against the parasite for visceral leishmaniasis (Leishmania infantum) with potential for treatment and vaccine development (Rondon 2011). Plant extracts shown remarkable insecticidal activity (larvicidal, ovoposition deterrent, inhibition of adult emergence) against mosquito larvae suitable for potential biological control uses (Elimam 2009). Ricinine has been isolated as an active insecticidal component of the plant against leaf-cutting ants (Atta sexdens rubropilosa) (Cazal 2009).
Venom antidote
Leaf flavonoids demonstrate insecticidal activity against stored grain pest (Callosobruchus chinensis) (Upasani 2003). Scorpion antivenom activity of plant extract (Uawibggyk 2006).
The fact that the leaves of the Castor Oil plant have galactagogic (milk-inducing) properties is a less well-known application of the herb: ‘The fresh leaves are used by nursing mothers in the Canary Islands as an external application, to increase the flow of milk’ (Grieve 1931). It once provided a vital medicament for nursing women in Africa, Malaysia and Indonesia – a tradition that has continued in some places. In 1880 the Queensland Government botanist FM Bailey wrote:
castor oil, but the leaves of the plant have been successfully used by Dr. Pringle as a galactopoietic [lactagogue].’ The doctor has reported two remarkable cases. The first one was that of a women who from total absence of milk in one breast, and a very limited supply in the other had lost two children in succession in early infancy. By the application of the castor oil leaves for about a week, the effect was truly astonishing, for the evil was remedied and the woman was enabled to rear her children afterwards. The second case was that of a delicate lady, who through the same simple application for three days was rendered capable of supplying the nourishment necessary for twins.
None of our naturalised plants have spread with greater rapidity over the colony than the castor oil plant, Ricinus communis, and if all accounts are true, few plants are of more value. Dr. Woolls in Contributions to the Flora of Australia, says:–‘Ricinus not only yields
Herbs with a similar lactagogue reputation include another weedy Australian import, the Purging Nut (Jatropha curcas). This herb was used in India for treating breast disorders, and to promote
A Lactagogue of Some Repute
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milk flow it was applied as a cataplasm to the breast. In Africa and the Cape Verde Islands the
leaf decoction was similarly recommended as a lactagogue (Iwu 1993; Quisumbing 1951).
Castor Oil plant leaves.
Jatropha curcas. (Image by JK Henning from www.Jatropha.org)
•
The chemical discoveries that resulted from the investigations of rotenone-based ichthyotoxins, as well as the poisons abrin and ricin, were associated with significant advances in understanding the complexity of some aspects of the Australian flora. There were, however, a number of other toxins whose poisonous properties were quite mysterious and extremely difficult to evaluate. One of the more famous disasters that marred the history of exploration across the continent was widely
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publicised following the fatalities of the Burke and Wills expedition in 1860–61 – an ambitious venture that involved crossing the continent from Melbourne to the Gulf of Carpentaria. Their tale involved a small aquatic water fern that the natives called Nardoo (Marsilea drummondii) – a story of toxicology that not only involved a number of the Pteridophyta (Fern Family), but also has some unanticipated links to neurological toxity due to insect larvae.
Chapter 9
POISONOUS PTERIDOPHYTA The Pteridophyta, or Fern family, tend to favour cool wet conditions, although there are some particularly hardy genera that have evolved to tolerate temperature extremes and extended dry periods – even under very arid conditions. Ferns are at their most profligate in the moist tropical regions of Australia, where around 65 per cent of the native species can be found. The northern wet tropics are of particular importance for two reasons – this region contains extremely ancient fern lineages representing the major evolutionary groups, and a high proportion of the ferns are endemic. These rainforest ferns can be particularly impressive – they include the Tree Ferns (genera: Dicksonia and Cyathea) and the ancient Giant Fern (Angiopteris evecta).
Cyathea cooperi, known as the Australian or Lacy Tree Fern, is native to New South Wales and Queensland - a very hardy and beautiful species that has spread in cultivation across the continent.
There are around 420 different fern species in Australia, the classification of which has changed dramatically over time. The literature can therefore be puzzling, with numerous species having an extremely similar appearance. Early records of the medicinal use of many ferns is relatively scarce and, apart from a number of well-known species, their identification has also been somewhat confused. Indeed, the following recent quote from the ‘Fern Pages’ of the Australian National Botanic Gardens and Australian National Herbarium (www.anbg.gov.au/fern) provides a good overview of the problem: The complexity and difficulty of the classification of the ferns and their allies is matched by no other group. After more than two centuries of work, the arrangement of species into genera and genera into families is still a long way from settled with almost every new treatment or flora adopting a different system to any that went before. A quick look at fern synonymy reveals a bewildering history of name changes in taxa at all levels as botanists struggle to find an arrangement that makes sense in terms of both the physical similarities of the plants and in terms of the
The Giant or King Fern, Angiopteris evecta, is fairly rare in Australia, although it ranges to the Polynesian islands and New Guinea. It is an impressively large plant that favours quite wet riverine and rainforest situations. 314
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Marsilea: A Toxic Water Fern
A rather unexpected food resource from the interior of the Australian continent came from Marsilea drummondii, an unassuming weed-like fern reminiscent of a four-leaf clover. Aboriginal people collected the sporocarps (fruiting bodies) to make a form of flour – a resource of inestimable value in this sparse, difficult environment, about which Dr Joseph Bancroft’s observations have tragic overtones: ‘Though Nardoo is pronounced by Baron von Muller to be a “miserable article of food”, the great value of it to starving travellers should not be lost sight of ’ (Bancroft 1884). A poignant comment indeed, especially in light of the disastrous failure of the Burke and Wills expedition in 1861, when all but one man starved to death. Dr Thomas Lane Bancroft (1894) noted the following additional details regarding its harvest and preparation:
Male Fern, from Koehler’s Medicinal Plants, 1887. Detailed botanical drawings are a means of providing meticulous portrayals of the various fern species. They can be invaluable in the process of identification. phylogenetic processes that led to the pteridophytes that we know today.
It is somewhat reassuring to know that everyone is in the same boat. Very few ferns have shown poisonous characteristics. There are a number with a known vermifugal effect that have been traditionally utilised as worm-removal remedies, notably the Male Fern (Dryopteris filix-mas) and a few related species in the northern hemisphere. These ferns would not have been taken on a regular basis, although the Male Fern was once official in many pharmacopoeias. A fern of some toxicological concern worldwide has been the ubiquitous Bracken (Pteridium spp.) – a weedy nuisance that has been responsible for incidents of animal poisoning. In Australia, the Nardoo fern (Marsilea drummondii), although edible, contained a secret poisonous hazard that provided an intriguing chemical puzzle for the early scientists.
In a day one could gather about a hundred-weight of the dried roots with involucres [a whorl of bracts beneath the flower] attached, from which perhaps forty pounds of involucres could be picked; ten pounds might easily be obtained daily by one person, which amount would be sufficient for a whole camp of blacks. Nardoo is not a wholesome substance eaten alone, but in addition to other food is a useful adjunct. At Annandale I had the opportunity to witness the gins [Aboriginal women] preparing Nardoo damper. The involucres, which are very hard, are pounded between two stones; a handful of them is held in the left hand and fed to a stone on the ground, a few grains being allowed to drop from the hand by separating, abducting the little finger, a smart blow being struck with a stone in the right hand, which effectually pulverises every grain at once; it is surprising with what rapidity they can do this work. The flour is mixed with water, kneaded to a dough, and baked in the ashes. The civilised blacks, who were supplied with wheaten flour from the station, were not too proud to make and eat Nardoo damper.
Sexual Advancements in the Fern World
The Marsilea ferns have earned a measure of botanical fame due to reproductive strategies that distinguish them as the most advanced of the living ferns. Nardoo can be found across the continent and, when massive flooding occurs, as
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The Marsilea genus contains about 65 species that favour floodplains or watery habitats. Six are Australian natives: Marsilea angustifolia, M. crenata (pictured here), M. drummondii, M. exarata, M. hirsuta and M. mutica. The best known of the Australian Marsilea is a small herb-like fern called Nardoo (M. drummondii). (Image courtesy: Réginald Hulhoven, GFDL, CCby-SA, Wikipedia)
Marsilea minuta. (Courtesy: Dan Pellegrini)
happened in 2010 and 2011, the herb finds this an excellent opportunity for propagation. Not only do the plants blossom and produce sporocarps (nut-like structures on stalks) on their rhizomes, they leave these capsules in the damp muddy soil once the floodwaters recede. The sporocarp packages, with a starch filling and spores intact, are left entombed in the dried mud, taking around three years to mature – although they can survive for up to 30 years, a perfect strategy for withstanding extended dry periods. Once the rains come, the starchy packing swells, the spores germinate and produce prothalli, which are either male or female, that release sperm or eggs. The fertilisation process leads to a small sporophyte and, ultimately, a mature Nardoo fern. It is this production of male and female prothalli (singular prothallus) that was the evolutionary advancement that made Marsilea the most advanced genus of all the ferns (Thomas 2007).
TH Johnston and JB Cleland provided further details of its culinary use in South Australia: ‘The sporocarps are pounded thoroughly between nardoo stones before the resulting coarse meal, mixed with water to make a dough, is cooked and eaten. This material, whose nutritive value is stated to be low, formed the main part of the vegetable diet on which [John] King, the sole survivor of the ill-fated Burke and Wills expedition, subsisted until rescued. He was supplied by the Yantruwunta people of the region’ (Johnston & Cleland 1948). Certainly, Robert O’Hara Burke and William John Wills were grateful for even this morsel on their disastrous excursion – although they did not find it particularly nourishing. Wills wrote in his diary just before his death: ‘I cannot understand this nardoo at all; it certainly will not agree with me in any form. We are now reduced to it alone, and we manage to get four to five pounds a day between us … It seems to give us no nutriment.’ Burke and Wills’ deaths were hastened by contracting beriberi, a disease that results from a dietary deficiency of thiamine. Unfortunately, the expedition was already suffering malnourishment from scant and deficient rations when they began to utilise Nardoo, as a diary entry recorded: Our legs almost paralysed so that each of us found it a most trying task only to walk a few yards. Such a leg bound feeling I never before experienced and hope I never shall again. The exertion to get up a slight piece of rising ground, even without any load, induces an indescribable sensation of pain and helplessness, and the general lassitude makes one unfit for anything. Poor Gray must have suffered very much, many times when we thought him shamming. It is most fortunate for us that these symptoms which so early affected him, had not come on us until we were reduced to an exclusively animal diet of such an inferior description as that offered by the flesh of a worn out and exhausted horse (Argus newspaper report, cited in Wilson & MacKinnon 1861).
Charles Gray had been the first of the party to die. Nardoo contains thiaminase – an enzyme that destroys vitamin B1 (thiamine), thereby compounding the nutritional deficiency. Unfortunately thiaminase is present in fairly high concentrations (significantly more than is found in Bracken1), which contributed to their untimely demise. The symptoms were devastating, with extreme effects on the nervous system – as Wills’
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diary described: ‘I still feel myself, of anything, weaker in the legs, although the nardoo appears to be more thoroughly digested … found myself altogether too weak and exhausted; in fact had extreme difficulty in getting across the numerous little gullies, and was at last obliged to camp from sheer fatigue … Starvation on nardoo is by no means very unpleasant, but for the weakness one feels and the utter inability to move oneself, for, as far as the appetite is concerned, it gives me the greatest satisfaction.’ Serious irreparable neurological degeneration can result from the consumption of an excess of thiaminase. Indeed John King, although he survived the expedition, developed permanent peripheral neuropathy and never regained the full use of his legs.
Map of Lake Eyre Basin, showing major river systems. (Courtesy: Map by Karl Musser, published by Wikipedia)
Diamantina River in flood. (Courtesy Sandra Brown, www. ga.gov.au, US Geological Survey Path 98 Row 77, acquired 13 January 2010)
Diamantina River crossing outside Birdsville, Queensland, a perfect habitat for the Nardoo fern. (Courtesy: Yeti Hunter at en.wikipedia) 1 The thiaminase activity in Bracken is 12–13.4 mg (per hour) by 100 g of tissue. Some fresh fish products also contain thiaminase. Raw carp entrails show a destructive value of around 10 mg of thiamine/100 g wet entrails (p/h), while the level in Anaphe insect larvae is estimated to be around 0.9 g thiamine lost per 100 g pupae (p/h) (Nishimune 2000).
NASA Image of Lake Eyre, 7 June 2005. The Lake Eyre Basin is a vast meandering water channel system covering more than a million square kilometres in Central Australia, involving four different states. The Diamantina and Cooper Creek run extraordinarily long distances draining from Queensland to South Australia, with the latter being the famous river system where Burke and Wills died. Sometimes, even with good rains, the waters will not reach Lake Eyre. Indeed, between 1990 and 2010 the systems were not connected. (Image courtesy: Goddard Space Flight Center’s Landsat Team and the Australian ground receiving station teams: landsat.gsfc.nasa.gov)
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Beriberi
Beriberi was first described from Batavia (now Jakarta) by Dr Jacobus Bintius in the early to mid 1600s in Medicine Indorum. At the time the city of Batavia was a disease-ridden pestilential mess, with an extraordinarily high incidence of fatalities that made it one of the most undesirable seaports on the planet. Most deaths were due to feverish conditions, notably malaria. With regard to beriberi Bintius noted: ‘This is a type of paralysis which the natives call beri-beri [which] … means sheep … with knees shaking, and their legs raised up [they] walk like sheep. It is a kind of paralysis, or rather Tremor for it penetrates the motion and sensation of the hands and feed indeed sometimes the whole body and produces tremors … There is a lassitude of the whole body’ (Chaffey, Australian plants online 2002). Beriberi not only results in paralysis and profound lassitude, there is fluid retention (oedema) associated with kidney and cardiac failure, palpitations, appetite loss, and respiratory distress. It would appear that Aboriginal people avoided the problem due to the great variety of native foods that they harvested. John MacPherson commented: As regards vitamin B, we have recently read of the natives of Central Australia being attacked by beriberi when they have abandoned their own native food of roots and other vegetable products for the civilized foodstuffs – white flour and decorticated rice. In the early days of colonization the white inhabitants suffered severely from scurvy, whereas the aborigines did not. A study of aboriginal diet would have averted that calamity. The natives of Port Jackson had many homely fruits which they consumed – for instance, native figs, wild raspberries, lilli pilli, the geebung, five-corner, native currant, native cherry, native grape and others. Probably these all contained vitamin C (MacPherson 1930).
Scurvy due to a lack of vitamin C was another nasty condition characterised by fatigue, a general feeling of illness (malaise), bleeding problems (particularly of the mouth) and loss of the teeth due to spongy gums. Jaundice, fevers and neurological complications can develop. There
were many more anti-scurvy and anti-beriberi dietary additions to the Aboriginal lifestyle – a culinary diversity that has been little appreciated for the greater part of the past two centuries
Ataxia from Silkworm Larvae
In the early 1990s it was noticed that a form of ataxia occurred on a seasonal basis in southwest Nigeria. Ataxia is a neurological disorder that results in muscular incoordination, which can be particularly evident with walking. A dietary link was suspected, which was later confirmed, when heat-stable thiaminase was found in the larvae of Anaphe venata, a butterfly that utilises Triplochiton scleroxylon as its food plant. The larvae, which provide a seasonal harvest in poor areas, have a food value similar to eggs – although the thiaminase activity is equivalent to that of Nardoo. Cooking the larvae does not detoxify the heat-resistant enzyme. The end result, in combination with a monotonous carbohydrate diet lacking B vitamins, is thiamine deficiency.
Female silkmoth with cocoon and eggs. (Courtesy: Merlin Crossley)
Silkworms. (Courtesy: Fastily at en.wikipedia CC-bySA-3.0)
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The discovery not only provided a medical solution, it also prompted an education program to rectify the problem. This issue was of particular scientific interest as it was the first report of insect-derived thiaminase. The edible larva of the Japanese Silkworm (Bombyx mori) also contains thiaminase, although the activity was less than one-third of that of Anaphe. Silkworms are less likely to be problematic because they are not usually incorporated into a thiamine-deficient diet (Nishimune 2000; Adamolekun 1997, 1994, 1993; Adamolekun & Ndububa 1994). Nardoo employs a few survival strategies that inherently protect its chemical integrity. The plant is well adapted to the extremely hot inland conditions and thiaminase is highly heat-resistant. Some idea of its resilience under these conditions was indicated in experiments undertaken by Baron von Muller more than a century ago, in 1861, which showed the fern could germinate from sporangia that had been boiled for 15 minutes. Even grinding and cooking the fern does not completely destroy thiaminase. Burke and Wills’ precarious nutritional predicament appears to have been compounded by the inclusion in their diet of freshwater mussels, some species of which, notably Velesunio ambiguus, contain thiaminase (Earl & McCleary 1994). Aboriginal methods of processing the fern tended to minimise its detrimental side-effects. The fact that they were roasted and then ground into a thin paste mixed with water and eaten using a mussel shell would have substantially diluted the enzyme activity.2 The overall leaching effect, and its combination with other nutrients (e.g. fish) in the diet, would have largely overcome the potential nutritional deficiency (Earl & McCleary 1994). Wills noted that their diet benefited greatly from the inclusion of vegetables: 2 The enzyme thiaminase requires the presence of amino acids (proline, hydroxyproline or adenine) to work. A diluted preparation of Nardoo would certainly have reduced, or even diluted out, the enzyme and these co-factors. Keeping the preparation out of contact with other organic material by using a mussel shell spoon would have further limited the availability of amino acids (Earl & McCleary 1994). The thiaminase activity of the Anaphe silkworm larvae has a similar reliance on protein substrates (amino acids) (Nishimune 2000).
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We were not long in getting out the grub [food] that Brahe had left, and we made a good supper off some oatmeal porridge and sugar. This, together with the excitement of finding ourselves in such a peculiar and almost unexpected position, had a wonderful effect in removing the stiffness from our legs. Whether it is possible that the vegetables can so have affected us, I do not know, but both Mr. Burke and I remarked a most decided relief and a strength in the legs greater than we had for several days. I am inclined to think that but for the abundance of portulac [Portulaca oleracea] that we obtained on the journey, we should scarcely have returned to Cooper’s Creek at all.
A very astute observation.
Nutritious Pigweeds
Portulaca oleracea. (Courtesy: Kim and Forest Starr, Hawaii)
Pigweed, or Purslane, is a heat and drought tolerant plant that is found throughout the Australian continent. It has an excellent
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reputation as an antiscorbutic and, in many places, was recommended for the treatment of scurvy. The succulent leaves and stems were a prized Aboriginal food item, while the seeds were collected from heaps of the plant that were left to dry: ‘The seeds, after washing, were ground between stones and consumed raw. They are highly nutritious and keep the natives in excellent condition’ (MacPherson 1930).
Purslane seed pods. (Courtesy: 6th Happiness, CC-bySA 3.0, Wikipedia)
Purslane has an ancient history of use across the globe, although in many places today it has been relegated to little more than an almostforgotten herb – and is even becoming locally endangered due to the perception that it is merely a useless weed. However, Purslane is a highly underestimated nutritional and medicinal resource. This unassuming weedy herb is a good source of carbohydrate (40.7%), protein (23.5%) and fibre (8%). It can also have a useful fatty acid content (5.3%; 8.5 mg/g net weight) that contributes omega-3 fatty acids to the diet, notably α-linolenic acid.3 It is rich in vitamin C (ascorbic acid), β-carotene and B vitamins (particularly B1, B2 and folic acid). Vitamin E levels may also be significant (α-tocopherol 230 mg/g dry weight) (Aberoumand 2009; Xin 2008; Simopoulos 2004; Liu 2000). Purslane can be a very good mineral resource (mg/100 g) (Brand Miller 1993): 3 Australian studies have determined the following: total fatty acid content of the fresh leaves (1.5–2.5 mg/g), stems (0.6–0.9 mg/g) and seeds (80–170 mg/g), with α-linolenic acid being present at high levels (% total fatty acid content) in the leaves (60%) and seeds (40% total). Beta-carotene levels in the leaves were also quite high (22–30mg/g) (Liu 2000). In comparison with other green leafy vegetables (mg/g), Purslane’s overall fatty acid level is high – e.g. Spinach (1.7 mg), Buttercrunch lettuce (0.6 mg), Red Leaf lettuce (0.7 mg), Mustard greens (1.1 mg) (Simopoulos 2004).
• The whole plant is low in sodium, with higher levels of potassium (709–940 mg), magnesium (206–266 mg) and calcium (97–112 mg). However, the root can be much higher in potassium (1170 mg) with good levels of magnesium (61 mg) and calcium (382 mg). Therefore while a damper (flour and water) preparation would be low in sodium, the levels of other minerals can be quite good: potassium, magnesium, calcium – as well as being high in iron (13–15 mg) and zinc (3–5 mg), and a low amount of copper. The leaf and seed paste levels can be • exceptionally high in iron (54 and 64 mg, respectively). • Portulaca pilosa can be equally high in iron (5.5–38 mg) and potassium (500–1000 mg); with reasonable amounts of sodium (50–120 mg), magnesium (170–300 mg), calcium (265–300 mg) and some zinc (1–1.7 mg).
Medicinal Marsilea
There are a couple of Asian Marsilea species which have a medicinal reputation. They include Marsilea minuta, which is an ancient Indian medicinal plant with a written tradition dating from around 100 AD. The fresh herb (leaves, plant) has sedative attributes and was traditionally utilised for insomnia and epilepsy. Marsilea minuta extracts have shown a nervous system depressive effect, as well as hypothermic activity (Parihar & Parihar 2006; Dixit 1974). Interestingly, a decoction of the whole plant has been recommended for spastic conditions involving the leg muscles. Some of these traditional uses appear to have a chemical basis because whole herb extracts have demonstrated significant anti-convulsive activity and potent sedative properties. The active principle, marsilin (or marsiline), was found to act by significantly increasing serotonin in the mouse brain.4 This suggested the potential use of the extract as an antidepressant remedy, with further studies providing support for its efficacy. An alkaloid isolated from Marsilea quadrifolia leaves has also shown central nervous system depressant properties and cholinergic 4 Serotonin affects the central nervous system function, with notable effects on mood, memory, learning capabilities and sleep.
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The leaf decoction of Marsilea minuta combined with ginger has been taken to treat coughing and bronchitis. The herb has often been employed as a remedy for insect bites, and the leaves are suitable for use as a vegetable (Parihar & Parihar 2006; Dixit 1974). (Image courtesy: Michael Kesl)
would contribute to their efficacy in skin infections. In particular, good antibacterial activity was demonstrated against Shigella (particularly S. boydii, S. dysenteriae, S. shiga), Pseudomonas aeruginosa, Staphylococcus aureus, Salmonella (S. typhi, S. paratyphi) and Bacillus (B. subtilis, B. cereus, B. megaterium) that would support its use in treating gastrointestinal and skin disorders (Ripa 2009). Marsilea trifolia appears to have a similar reputation in Bangladesh, with recent studies indicating good analgesic and antipyretic activity, the latter supporting its use as a febrifuge in traditional medicine (Khan 2011).
Water Ferns for Environmental Remediation
Marsilea quadrifida. (Courtesy: Krzysztof Ziarnek)
activity – although it did not reveal narcotic activity (Bhattamisra 2008; Mukhopadhyay 1995; Satyavati 1986; Siddiqui & Husain 1991; Chatterjee 1963). Other investigations have shown extracts possessed potent cholesterol and triglyceride lowering effects: decreased deposition of fatty deposits, dissolution of atheromatous plaques and increased faecal excretion (Gupta 2000). The Asian Marsilea quadrifolia is another edible aquatic species with a medicinal reputation – it is considered to have anti-inflammatory, diuretic and febrifugal properties. A plant decoction was taken to treat fevers or reduce oedema. The herb was utilised as a tonic (cooked with meat) in menstrual problems, leucorrhoea (vaginal discharge) and eye disorders. The fresh leaf juice has been employed as an antidote to snakebite, and applied externally as a healing agent to ulcers and abscesses. The fern ointment was also applied locally for heat rash (Perry & Metzger 1981). The plant has shown potent antioxidant, antimicrobial and cytotoxic potential. Some extracts possess antibacterial and antifungal properties that
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Marsilea in water-inundated habitat.
Water Lettuce (Pistia stratiotes).
Water plants such as Marsilea have attracted recent attention for their potential anti-pollutant actions. Numerous species have demonstrated an ability to concentrate heavy metals or minerals, facilitating their removal from contaminated wastewater. Indeed, Marsilea ferns and the Water Hyacinth (Eichhornia crassipes) growing along effluent channels can concentrate copper and calcium, as well as mercury. Other aquatic plants with remedial mercury-removal effects include Duckweed (Spirodela polyrhiza), Floating
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Primrose Willow (Jussiaea repens), Kodo Millet (Paspalum scrobiculatum), Water Lettuce (Pistia stratiotes), Temple Plant (Hygrophila schulli), Monochoria hastata and Water Hyssop (Bacopa monniera). Mercury-accumulating species include Purple or Red Nut Sedge (Cyperus rotundus), Chloris barbata and Bermuda Grass (Cynodon dactylon), as well as Cabbage (Brassica oleracea) and Amaranth (Amaranthus oleraceus) (Skinner 2007; Barman 2001; Lenka 1992). Duckweed, Water Hyacinth, Monochoria vaginalis and Azolla pinnata have also shown arsenic-retentive properties that could be useful for phytoremediation in countries such as Bangladesh, where arsenic-contaminated water supplies are a serious problem. Male Fern (Dryopteris filix-mas) was likewise effective in the bioconcentration of arsenic from soil samples (Mahmud 2008).
Marsilea villosa is an endemic Hawaiian species known as the Villous Waterclover. This image shows the four-leaf clover appearance that characterises these ferns and their preference for a watery habitat. (Courtesy Kim and Forest Starr, Hawaii)
cattle. Studies eventually established that the fern was safe for grazing for limited periods (up to 10 days), as long as it was not used again for the following three weeks. An increase in toxicity was found to occur on a seasonal basis – which was greatest during summer when the plant underwent vigorous growth. The activity of thiaminase from Nardoo was substantially more than that recorded for a couple of other ferns with known toxic potential – i.e. Bracken, Pteridium aquilinum (Nardoo was up to 100 times more potent) and the related Rock or Mulga Fern, Cheilanthes sieberi5 (Nardoo was four times more potent) (Potter & Baird 2000; Dowling & McKenzie 1993; Everist 1981; McKenzie 1978; Clark & Dimmock 1971). The toxicity of the Mulga fern (Cheilanthes sieberi) has been linked to the carcinogen ptaquiloside. It appears that other fern relatives such as Dryopteris juxtaposita have similar toxic potential (Kumar 2001; Gounalan 1999; Kataria 1998; Smith 1989). (Image courtesy: Peter Woodard)
5 Some reports have listed this species as Cheilanthes tenuifolia, which appears to have been a misidentification.
Toxic Variability
A Mysterious Toxin
Nardoo is generally grazed by animals without causing illness. However, there are times after heavy rains when it may be the only food available and stock casualties tend to occur. Nardoo has been associated with the development of ‘staggers’ (staggering gait) in sheep, as well as gastroenteritis, liver and kidney congestion and death on long treks. Sheep poisoned by Nardoo can develop brain abnormalities (cerebrocortical necrosis or polioencephalomalacia). A haemorrhagic syndrome similar to Bracken poisoning has also been seen in
Pteris cretica, Cretan Brake. (Image courtesy: Kim and Forest Starr, Hawaii)
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Left: Pteris cretica, Cretan Brake. (Image courtesy: Kim and Forest Starr, Hawaii)
Right and below: Pteris excelsa, Waimakanui. (Images courtesy: Kim and Forest Starr, Hawaii)
Ptaquilosides have been found in numerous species of Pteris (P. cretica, P. dispar, P. excelsa, P. fauieri, P. nipponica, P. oshimensis, P. purpureorachis, P. ryukuensis, P. semipinnata, P. treula, P. wallichiana), but the Indian species P. stannophylla did not contain any of these toxins. Many other ferns contain these compounds – for example, analogues were present in Hypolepis punctata (hypolosides) and Dennstaedtia hirsta (hypolosides, dennstoside A) (Somvanshi 2006; Potter & Baird 2000; Saito 1989a, 1989b). A review of 40 Indian pteridophytes found that only Onychium contiguum, a plant grazed by cattle in high-altitude regions of the Himalayas, contained high ptaquiloside levels (499–595 mg/kg). This herb has also shown experimental
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carcinogenic activity. The level in samples of the same fern from other areas (e.g. Mukteswar) was low (0.68 mg/kg) – suggesting substantial variability in its toxic potential. Diplazium esculentum, Polystichum squarrosum and Dryopteris juxtaposita had a moderate ptaquiloside content (19–31 mg/kg). Very low levels (0–0.4 mg/kg) were found in Cheilanthes farinosa and Christella dentata, while none was present in Adiantum incisum (Somvanshi 2006; Dawra 2001; Gounalan 1999). This research illustrates how prevalent this carcinogen is in ferns, and the great variability in its toxic potential. Other ptaquiloside-containing genera include the following (Potter & Baird 2000; Saito 1989b): Cheilanthes (C. myriophylla) Cibotium (C. barometz) Coniogramma (C. gracilis, C. intermedia, C. japonica) Dennstaedtia (D. distenta, D. hirsta, D. scabra) Histiopteris (H. incisa) Hypolepis (H. bamleriana, H. tenuifolia, H. punctata) Microlepia (M. marginata var. bipinnata, M. strigosa) Monachosorum (M. arakii, M. flagellare) Onychium (O. japonicum) Pityrogramma (P. calomelanos, P. sulphurea) Sphenomeris (S. chusana).
Medicinal Uses of Cheilanthes Ferns Cheilanthes ferns are often found in rocky crevices. They can withstand long periods of dryness, curling up to await the reviving effects of rain – hence, they are often called ‘resurrection ferns’. This gives species like the Woolly Cloak Fern, Cheilanthes lasiophylla, pictured here, the ability to be distributed throughout the drier parts of the continent, ranging from Western Australia through Central Australia into South Australia and New South Wales.
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In Australia the Cheilanthes genus contains around twelve species, including a couple of species that were formerly included in the genus Notholaena. In addition to the Rock Fern (Cheilanthes tenuifolia), those of a tropical habit include C. brownii, C. caudata, C. contigua, the Bristly Cloak Fern (C. distans), C. nudiuscula and the Mulga Fern (C. sieberi). Other Australian species include the Woolly Cloak Ferns (C. lasiophylla and C. vellea), C. prenticei, C. pumilio and C. sciadioides. The Cheilanthes genus is not particularly well known for its medicinal potential, although a few species have had limited uses overseas. The Rock (Bush) Fern, Cheilanthes tenuifolia, is a small creeping plant that dies down during the dry season, regenerating during the wet season storms. The plant has a delicate scent and was decocted for use as a hair wash, similar to the use of the Maidenhair Fern. Rock Fern has been used as a component of dye mixtures by the New Zealand Maori (Riley 1994). A Malaysian dusting powder for newborn infants combined Rock Fern (Cheilanthes tenuifolia) with Hedyotis hispida, Biophytum and a wild pepper. In Fiji a leaf tea from the Rock Fern was given to children for stomach pains, while in India the rhizomes and roots were used to make a general tonic (Riley 1994; Burkill 1935). Some species have been utilised as wound-healing remedies. In Nepal the frond juice from Cheilanthes albomarginata was applied to cuts and wounds (Manandhar 1995). An infusion of an American species, Cheilanthes wootoni, has even been applied to gunshot wounds. The herb also appears to have been highly regarded by American Indian tribes as a ‘life medicine’ (Moerman 1986).
A number of other species have had minor medicinal uses: • USA (California): Cheilanthes covillei stems and leaves brewed as a ‘squaw tea’ (probably used as a diuretic or tonic) (Zigmund 1981). • USA (southern states): Cheilanthes tomentosa infusion (stem and leaf ) for urinary disorders (Ford 1975). • Mexico: Cheilanthes kaulfussi tea taken as a remedy for lung problems (Ford 1975). • Ecuador: Cheilanthes chrysophylla (plant infusion) was utilised as an astringent and urinary stonedissolving remedy (Varea 1922). • Chile: leaf infusion of Cheilanthes pruinata provided a remedy for fevers (Aldunate 1983). • Africa: powdered root of Cheilanthes hirta was used as an anthelmintic for tapeworm by the Zulu (Watt & Breyer-Bradwijk 1962). • Africa (Lesotho): Cheilanthes hirta was mixed with ginger and taken as a remedy for a sore throat. Cheilanthes eckloniana was burnt to prepare an ash that was applied to sores, particularly those that had become infected (Zepp 1982). • Nepal: a number of species have been utilised as a remedy for gastric troubles, notably peptic ulceration: Cheilanthes albomarginata, C. anceps (with Drymaria diandra), C. bicolor and C. tenuifolia. The plant juice (frond juice: dose 6 teaspoons) was taken 2–3 times daily. C. rufra juice (2 teaspoons) was also recommended 3 times daily to relieve indigestion (Manandhar & Manandhar 2002; Manandhar 1993). • Indian traditions: plant decoction of Cheilanthes albomarginata and C. farinosa recommended as a remedy for chest pain (Kamble 2010).
The Zulu medicinal plant Cheilanthes viridis was utilised for wound healing – dried and powdered for use, or fresh crushed fronds poulticed on the site. This species possessed good antibacterial properties (Kelmanson 2000). (Image courtesy: Kim and Forest Starr, Hawaii)
Interesting new avenues of research have emerged for a few of these traditional remedies. Studies of Cheilanthes dalhousiae, a species utilised medicinally in Himalayan India, indicated broad-spectrum antibacterial activity (Bacillus subtilis, Escherichia coli, Pseudomonas aeruginosa and Staphylococcus epidermis). The fern frond extracts contained a number of flavonoids (Mishra & Verma 2010). This would lend support to the traditional use of a rhizome paste for treating boils and ‘ruptured skin’ (Manandhar & Manandhar 2002). There are other traditions that suggest these herbs have antibacterial properties. The leaf extract
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(mixed with honey) of Cheilanthes albomarginata was taken after meals as a remedy for tuberculosis. This herb has a reputation as a good general tonic for children and weakened individuals (Parihar & Parihar 2006). Cheilanthes anceps was similarly employed for respiratory disorders (tuberculosis, cough, asthma) and as an anti-inflammatory for joint pain. Extracts were shown to contain flavonoids with antioxidant activity (Chowdhary 2010). Cheilanthes glauca has been utilised as an anti-inflammatory and antidiabetic remedy in Chilean traditions.6 Flavonoid-containing extracts (particularly those with good rutin levels) were shown to have potent antioxidant properties with potential anti-cataract activity (Pastene 2007). In addition, Cheilanthes contracta has been employed as an anticancer remedy in Africa (Charlson 1980). Although this recommendation appears to be at odds with the carcinogenic activity of some other species in the genus, recent investigations of the Indian medicinal herb Cheilanthes farinosa focused on its anticancer potential. The plant has been traditionally utilised for treating liver disorders and has shown anticancer (antiproliferative, apoptosis-inducing) activity in human liver cancer cells (Radhika 2010). Other studies have shown anti-inflammatory and analgesic activity for extracts of this herb – which tends to support its use in Ethiopia as a remedy for inflammatory skin disorders. While a number of compounds were isolated with pharmacological properties – the flavonoid rutin, and cinnamic acids (caffeic acid and chlorogenic acid) – only chlorogenic acid possessed strong anti-inflammatory and antinociceptive effects (Yonathan 2006). 6 Other ferns have useful antidiabetic properties. Studies of Dryopteris species utilised in Mongolian medicine for the treatment of diabetes demonstrated improvements in glucose utilisation and insulin resistance in diabetic rats (Khookhor 2007).
The Bothersome Bracken Botanical Conundrums? Serious debate has dogged the botanical classification of Bracken – whether the genus contains a number of distinct species, or a single species with many subspecies and varieties. In general, Pteridium aquilinum subsp. aquilinum
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Pteridium aquilinum from Bilder ur Nordens Flora, CAM Lindman, 1917.
belongs to the northern hemisphere (where eight varieties have been proposed) and Pteridium aquilinum subsp. caudatum (with four varieties) is restricted to the southern hemisphere. The variety aquilinum is primarily found in the British Isles. There is, however, the variety latiusculum (sometimes classified as a subspecies) that favours the northern boreal forests (including the ancient pine woods of Scotland), and the subspecies atlanticum from the Atlantic fringes of western Scotland – while variety caudatum is a pasture weed in the Caribbean (Pakeman & Marrs 1993). Opinions can differ widely. Proposals have been made for the following varieties of Pteridium aquilinum to be raised to species status: africanum, aquilinum, arachnoideum, decompositum, esculentum, latiusculum and revolutum – with the
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Pteridium aquilinum subsp. decompositum. (Courtesy: Kim and Forest Starr, Hawaii)
varieties pseudocaudatum and pubescens as varieties of P. latiusculum (Thomson & Alnoso-Amelot 2002; Thomson 2000). It is important to realise that in northern Australia the two species from the northern and southern hemispheres overlap. Currently, three Australian taxa have been accepted (Brownsey 1989): • Pteridium aquilinum. • Pteridium esculentum (P. aquilinum subsp. caudatum var. esculentum). • Pteridium revolutum (formerly classified as P. aquilinum subsp. aquilinum var. wrightianum) which is found in northern Queensland and the Northern Territory. P. aquilinum var. lanuginosa, which was erroneously reported from northern Queensland in the early literature, is now considered to be P. revolutum. • There is also a hybrid form, Pteridium esculentum x P. revolutum: a wild ‘Northern Bracken’ hybrid that has been variously classified as Pteridium x semihastatum and P. aquilinum var. yarrabense (P. aquilinum subsp. caudatum var. yarrabense) and later classified as P. semihastatum. Bracken also has the potential to be confused with some non-poisonous ferns such as the False or Mountain Bracken (Culcita dubia) in Australia.
Of all the ferns utilised as food or medicine, the northern hemisphere Bracken (Pteridium aquilinum; Pteris aquilina in older literature) would be one of the most widespread and extensively employed throughout the world. The southern hemisphere equivalent, Pteridium esculentum, is common throughout Australasia, New Zealand and the Pacific Islands. The fern has had a range of diverse uses, although these are generally no longer of any major practical value. The roots of Male Fern (Dryopteris filix-mas) and Bracken were even occasionally substituted for Hops in making beer. A distillation of the stem and leaf provided a ‘root’ beer with supposed tonic virtues. In Siberia the roots were combined with about two-thirds their weight in malt for the same purpose. Bracken and Male Fern have been variously prepared to make lye and glass due their high silica content, and contain enough tannin to be used as a tan for the production of leather. Bracken fronds, surprisingly, also make a durable thatch.
Green glass. (Courtesy: Melissa Robinson)
Lye, Glass and Shampoo
Ferns once made a substantial contribution to the production of numerous common household products. Until the mid-1800s fern ash was used to launder clothing and in the preparation of lye (a mixture of fern ashes and water). The latter often favoured the use of Maidenhair ash. Since Roman times, ferns have been extensively used in glass manufacture. Maidenhair and Bracken contain large amounts of carbonate of potash, which provided the alkali salts needed to produce
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attractiveness. The ash, or lye, prepared from Maidenhair (Adiantum species) was used almost everywhere the fern was found, although a few other ferns such as the Black Spleenwort (Asplenium adiantum-nigrum) had a similar reputation. Not only did they provide a shampoo or hair wash, but they were thought to prevent hair loss, cure dandruff and encourage a lustrous thick growth. Davallia tenuifolia, the leaves ashed and mixed with sesame oil, was reputed to preserve hair colour (i.e. prevent greying). The Wall Rue (Asplenium ruta-muraria) was also recommended: ‘The lye made thereof is singularly good to cleanse the head from scurf and from dry and running sores, stays the shedding or falling of the hair, and causes it to grow thick, fair and well-coloured, for which purpose boil it in wine, putting some smallage-seed [a type of celery] thereto and afterwards some sesame oil’ (Grieve 1931). In China, an oil made from the roots of Polypodium hastatum infused in Sesame oil was a hair growth promoter. Maidenhair Fern, from Ferns of Great Britain and Ireland, Thomas Moore and John Lindley, 1867.
glass. Bracken was so widely used that in France a thick, dark coloured glass called verre de fougère (Bracken glass) was used for wine glasses. Maude Grieve (1931) mentioned some other practical aspects of the fern: ‘The potash yield of Bracken ash is so considerable that in view of the present scarcity of fertilizers, this source of supply is well worth attention. Potash is a particularly valuable fertilizer for potato and sugar-beet land, especially for light loams and gravels and sandy soils. It should be borne in mind by persons having access to quantities of Bracken, that they have a usable supply of this almost indispensable manure at hand, either for cultivating flowers or crops, at the expense of a little trouble.’ The ash from the green plant was regarded as being more valuable than that from withered or dried fronds. The yield from 50 tons of dried fern was 1 ton of potash. In addition, numerous ferns have been used as tonic agents to promote hair growth and
Maidenhair Fern (Adiantum species).
Adiantum capillus-veneris. (Courtesy: Tony Rodd, flickr)
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Maidenhair Fern, which is found throughout mainland Australia, is one of the eight native species of Adiantum. In many parts of Australia Adiantum aethiopicum (pictured here) was utilised as a remedy for respiratory disorders (Lassak & McCarthy 1992). (Image courtesy: Peter Woodard)
In Indonesia the small Rock (Bush) Fern (Cheilanthes tenuifolia) was used as an alternative to Maidenhair for making a hair tonic (the whole plant made into a decoction). It belongs to the same family – the Adiantaceae. Other ferns likewise used as hair tonics and rinses in Indonesia and Malaysia included Asplenium nidus, Lycopodium phlegmaria, L. laxum and Ribbon Fern (Ophioglossum pendulum) – the latter infused in oil. In the Amazon, Lycopodium funiforme had a similar reputation, as did the Five-finger Fern (Adiantum pedatum var. aleuticum) in India (Hirschhorn 1983; Schultes & Raffauf 1990). American Indians used the ash of the Five-finger Fern rubbed into the hair to enhance their shiny black braids. Frond infusions of the Wood Fern (Dryopteris dilatata) provided a useful hair wash, while an infusion of the
Lygodium japonicum. (Courtesy: Wikipedia CC-by-SA-3.0)
Marshman,
Sword Fern (Polystichum munitum) was reputed to cure dandruff (Lloyd 1964). Actinopteris dichotoma also provided a dandruff remedy – the rhizome boiled to make a wash – in the West Indies (May 1978). Interestingly, some of these traditions may of practical benefit. A recent study demonstrated hormonal (anti-androgenic) activity for Lygodium japonicum spores that promoted hair-growth in animals (Matsuda 2002).
An Unaccommodating Neighbour
Bracken furnishes an excellent example of how poor management of natural resources can easily provide hardy weeds with valuable invasive opportunities. Bracken has a fire-tolerant rhizome that allows the fern to readily regenerate. Destructive farming practices, drainage works and fallow lands provide excellent opportunities for this invasive weed to take over. Farmers thereby lose productive land as the clearing/control costs per annum can become astronomical. Equally disturbing is the effect that Bracken invasions have on the integrity of native forests, where the natural regeneration process is suppressed. Additionally, Bracken harbours tick pests that kill young birds and infect sheep – a nuisance plant with deadly potential for wildlife. Bracken is a resilient, hardy weed that deploys some very clever survival strategies. It has the highest rate of photosynthesis of any fern – an attribute exploited by the plant to produce rhizome starch reserves that permit a vigorous growth habit. The fern can opportunistically colonise the poor acidic soils that are common around waste sites (landfills, clearings, roadsides), although water-inundation naturally deters its spread. The fern’s ability to thrive on nutrient-poor soils is largely due to a streamlined recycling system that translocates nutrients from dying fronds to the rhizome at the end of the growing season. These are re-used for new frond growth when the opportunity arises. Indeed, Bracken readily spreads to fertile ground, crowding out the local vegetation. Bracken is not an accommodating neighbour. Dense stands of the live fern provide little opportunity for competing plants, while Bracken leaf litter is resistant to decay, covering the ground in layers up to 60 cm thick (Pakeman & Marrs 1993).
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Compromising the Microclimate
Bracken is usually a prolific weed, as shown on the left; however, where the tree canopy limits accessibility to light, growth patterns are restricted.
Bracken can have a far greater environmental impact than one would initially appreciate. Colonisation results in a level of microclimate change. The mature fronds provide a substantial covering overhead that limits light penetration into the understorey below. The Bracken covering disturbs water distribution patterns by intercepting around 50 per cent of rainfall, which does not reach the soil below. It also tends to increase transpiration, resulting in higher evaporation rates. Overall a reduction in water supply results – a situation that can be disastrous for the local vegetation, particularly on sites already experiencing water shortages. If this were not enough to severely limit opportunities for native seedling growth, Bracken actively produces chemicals (allelopathic agents) that are washed out of the leaf litter. They act to inhibit germination and the growth rate of any seedlings in the vicinity will be slowed (Pakeman & Marrs 1993).
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grasses and legumes. Burning simply encourages the fern’s growth, which usually occurs at the expense of the more useful native grasses (Everist 1981). This extract from Poisonous Plants: A Field Guide, by RM Dowling and RA McKenzie (1993), provides a good summary of the situation: ‘The control of bracken infestation of pasture is very difficult. A program of pasture improvement combined with measures to reduce the vigour of the bracken is probably the most effective approach. Slashing each time a new crop of fronds uncurl may help … Bracken can be relatively resistant to herbicides. Continued research worldwide means that recommendations for bracken control using herbicides change frequently.’ One of the simplest methods of controlling Bracken is to plant trees. Once the tree canopy is taller than the Bracken canopy it can suppress the growth of the fern.
A Controversial Food Resource
Surprisingly, the Bracken fern has long provided a food resource across the globe. The cooked fronds can be used to make a sharp-tasting spinach-like dish, albeit somewhat slimy and stringy. Bracken was once a popular food resource in Japan and the Philippines, as well as being employed in some parts of Africa, Europe and America. A note in an old Technical Manual of the US War Department on ‘Emergency Food Plants and Poisonous Plants of the Islands of the Pacific’ made the following observations on Bracken’s food value: Parts of certain species of fern are regularly used as food by the natives and these parts are offered for sale in native markets. In Angola the indigenous people of certain regions use fern as food. While the food value of edible parts of ferns is probably relatively low, yet these parts will help sustain life when other foods are not available. In general, the parts most commonly used are the young unfolding leaves, commonly spoken of as ‘fiddle-heads’; these may be eaten either raw or cooked. Some of these ‘fiddle-heads’ are too tough, others bitter or otherwise bad tasting. But one point may be kept in mind that, as far as is known, none of the ferns is actually poisonous when eaten (Watt & Breyer-Brandwijk 1962).
Understandably, Bracken has long been an unwelcome weed for farming concerns. The plant is a formidable adversary. Bracken-invaded pastureland presents an extremely difficult eradication problem. Herbicides tend to kill only the top of the plant. Most treatments cannot kill the roots without causing serious injury to the soil and the local environment. The conditions that fostered the original invasion In New Zealand the Maori made extensive use need to be radically altered for any chance of success of Bracken (Pteridium aquilinum var. esculentum). – a labour-intensive and costly venture that involves The young coiled shoots had their hairy covering ploughing, fertilising and replanting with pasture removed and were boiled for an hour before use.
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Young coiled fern shoots are called fiddleheads because of their resemblance to the scrolled ends of a violin. On the left, Cyathea cooperi fiddleheads. On the right, Angiopteris evecta.
The preparation of the fresh roots was a more lengthy process, however. They were dried, soaked in water, and re-dried before finally being roasted and ground to make a type of flour. The product does not appear to have been particularly savoured, although opinions differed. Some compared it to newly made bread, or to coarse ship’s biscuits, while others were rather less complimentary. In 1842 Aubrey commented that ‘a very good imitation might be made with a rotten stick, especially if slightly pounded, to which it bears a striking resemblance, both in taste and smell’ (Crowe 1990). Even so, when eaten before sea voyages the root was reputed to prevent sickness. Joseph Banks considered the prepared meal to be barely palatable, commenting that it possessed ‘a sweetish clammyness … not disagreeable to the taste; it might be esteemed a tolerable food was it not for the quantity of strings and fibres in it, which in quantity three or four times exceeded the soft part; these were swallowed by some but the greater number of people spit them out, for which purpose they had a basket standing under them to receive their chewed morsels.’ The impression appears to be of a somewhat less-thansavoury culinary experience. Certainly the type of preparation and quality of the harvest seriously influenced the desirability of the end product. The more fibrous roots could be beaten to a pulp and the strands removed, leaving only the
Fiddlehead sculpture by James W Boyd, 2001, located in front of the Saint John Arts Centre in Saint John, New Brunswick, Canada. Boyd commented: ‘I chose to create a large stylized fiddlehead in granite because I find it a beautiful form. I love the fact that the actual fiddlehead is only around for a few weeks before it transforms or grows into a fern. When I think of something that represents my province the fiddlehead comes to mind … They grow along the rivers here in New Brunswick and many people pick them in the early spring for their supper tables. They are also found in grocery stores and markets during the season. The First Nations peoples have a long tradition of picking the fiddleheads. They are great to eat steamed and there is a lot of different recipes for fiddleheads. I even had deep fried fiddleheads in a local bar earlier this year.’ Australian Aboriginal tribes and New Zealand Maori have also held fern resources in similar esteem. The Fiddlehead sculpture is about 2 metres tall, made in granite from Quebec, Canada in 2002. (Image courtesy: Michael Stewart)
starchy residue for making cakes – although this was quite a labour-intensive enterprise. The result was considered to be useful travel provender that could be taken with honey or other additives to enhance the taste. In 1846 Thomas Brunner made the following rather complimentary observations regarding Bracken in the Maori diet: ‘The natives prepare a very palatable dish of Ti [cabbage tree] and fern root. They extract the sweet particles of the former by beating and washing it in a proper quantity of water, and when about the consistency of honey they soak in the liquid some layers of well-beaten and cooked fern-root, which, when properly moistened, is eaten, and has a similar relish to gingerbread.’
Discovery of a Dietary Carcinogen
There is, however, another thread to the story of Bracken that came as a great surprise to the scientific world in the 1960s. The Japanese had long prized Bracken for culinary purposes and it therefore came as something of a shock when studies indicated that the
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who spent their childhood in Bracken-infested areas, in contrast to those who had not – an incidence that was 2.34 times higher than for non-residents (AlonsoAmelot & Avendano 2002; Galpin 1990; Hirono 1972).
Environmental Influences on Toxin Levels Bracken ferns near Flagstaff, Arizona, USA. (Courtesy: Tylerfinvold, GFDL, CCA-by-SA 3.0)
fiddleheads contained toxins with strong carcinogenic potential. The first report, which was published in Nature in 1965 by IA Evans and J Mason, detailed an incidental finding that quickly rang alarm bells regarding the fern’s dietary use. The discovery was quite accidental. On feeding two rats the fern as a treat, researchers noted the development of a uterine tumour. While this may have been a coincidence, it led to them to expand the scope of the experiment. Forty rats were given Bracken powder (34%) as part of their diet for around two months and observed for almost a year. The results were unexpected, with a startlingly high incidence of tumours. Comparison with the control group, which had not been fed Bracken and remained in good health, highlighted the problem. More worrying news was to follow. Investigations indicated that other animals could be affected: sheep, hamsters, guineapigs, Japanese quail and Egyptian toads (Trotter 1990; Asano 1989). The possibility that the incorporation of Bracken in the Japanese diet could be associated with the high rate of some forms of cancer quickly instituted further research. Studies in Japan and Brazil determined a close relationship between the dietary use of Bracken and cancer of the upper alimentary tract. In Japan, oesophageal cancer was found to be 2.7 times more common in individuals who regularly ate the fern. Other investigations showed a significant increase in the risk of gastric and oesophageal cancers in communities sited near Bracken-infested areas – particularly in Brazil, Venezuela, Colombia and Costa Rica. In Gwynedd (Wales) there was a strong association between cancer development in those
It should be noted that the rate of incidence of gastric cancer has been definitely linked to a regional influence. For instance, the rate (per 100,000 population) in Japan is 77.9, while in northern Africa it is 5.9. In northern Italy, the incidence is also high at Cremona (78.4), while Genoa (120 km distant) has less than 20 cases of stomach cancer per 100,000. Although certainly dietary influences (including nutritional status, vitamin and mineral levels) play a role, there is no current comprehensive explanation for the differences. There are other influential considerations that are likely to play a role: infection with Helicobacter pylori (a strong carcinogenic risk factor), cigarette smoking and industrial pollutants (which can have a significant impact), and some dietary habits. In addition, nitrate contamination of water supplies has been established as a risk factor in Colombia (See Alonso-Amelot & Avendano 2002 for a more detailed discussion).
The findings in Wales posed the possibility that the carcinogen could be transmitted through unprocessed cow’s milk. Prior to 1940 rural families had grazed milkproducing cattle on Bracken-contaminated lands and the milk was sold direct to the local community. These practices later changed with bulk milk collection and the introduction of processing, which coincidentally lowered the risk of exposure. Unfortunately, while the contamination of milk had already been suspected, the high carcinogenic potential of buttermilk was not truly appreciated. The conundrum is that milk can concentrate the water-soluble toxin, while butter, cream and cheese (which have a higher fat content) do not. The practice of keeping buttermilk for home use by dairy farm families could have inadvertently
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increased the risk of exposure, particularly for children. Buttermilk would not have been exposed to the diluting effect of the processing that occurred with communal milk-supplies (Ravilious 2004; Trotter 1990; Galpin 1990). Studies also found that the incidence of gastric and oesophageal cancer was three times greater in parts of Costa Rica where Bracken was incorporated into the diet of cows. Experimental animals fed milk from Bracken-fed cows were shown to develop cancer. The implications became a matter of serious concern, even in countries such as the United Kingdom where dietary habits no longer involved direct ingestion of the carcinogen. However, during the latter decades of the twentieth century changes associated with modernisation in animal feed and milk processing ensured that contamination with the fern was a relatively low risk in many, but not all, countries (Alonso-Amelot & Avendano 2002; Shahin 1999; Trotter 1990). There are other considerations that were found to exert an influence on the situation. The differences in the incidence of carcinogenicity in various parts of Japan seemed to be related to location, which appeared to alter Bracken’s toxicity. The part of the plant used and the growing season were also found to significantly influence the experimental results. The carcinogenic activity was greater in the young curled fiddleheads than in the stem, while that of the root was higher than the young fronds. The incidence of tumours and death was more prevalent in animals fed the young fern as opposed to the mature fern – although the latter was not without detrimental effects. The magnitude of the toxicity therefore differed substantially. Shikimic acid, one of the first carcinogenic compounds identified, was shown to cause gastric cancer and leukaemia in mice, but not rats. Other toxins were present, including the cyanogenetic glycoside prunasin. However, the cyanide (HCN) poisoning that could have been expected to occur with this compound did not manifest in the studies. This was interesting from a chemical point of view. Bracken’s prunasin levels could be quite variable and the herb was found to demonstrate ‘biochemical polymorphism’ – that is, while prunasin was present in most populations, some populations lacked this compound and/or the enzymes needed to liberate
HCN (Trotter 1990; Hirono & Yamada 1987; Hodge 1973; Hirono 1972; Bennett 1968). The carcinogenic potential of Bracken (Pteridium aquilinum, P. esculentum, P. revolutum) was finally validated on a chemical basis when a highly potent, but extremely unstable, toxin was discovered in 1983. It was named ptaquiloside (an illudane compound), and the highest amounts were found in the crosiers and young unfolding fern fronds. Australian studies showed that highly variable levels of the carcinogen could be present, ranging from 0 to 12,945 mcg ptaquiloside/g. This would explain variations in Bracken’s toxic effects in animals. Of 91 Australian samples studied, 57 per cent contained more than 1000 mcg ptaquiloside/g, with 15 per cent rating more than 5,000 mcg/g (Smith 1989, 1994; Hirono & Yamada 1987).
The Genus Polystichum The Polystichum genus contains a fairly large number of ferns (around 260 species) that have a preference for rocky sites. The largest diversity occurs in eastern Asia, with at least 120 species being found in China. Another 100 are found ranging from Mexico to Polystichum fern. (Court- Brazil. Various species been utilised esy: Kim and Forest Starr, have medicinally, although Hawaii) some are suspected of containing ptaquiloside. Indeed, Indian studies of Polystichum squarrosum have shown that it had toxic effects in animals resembling Bracken poisoning (Sivasankar & Somvanshii 2001). In New Zealand, Richard’s Shield Fern (Polystichum richardii) provided a vegetable, the new shoots (fiddleheads) being steamed similar to asparagus (Crowe 1990). A few species have also been utilised therapeutically overseas. In Africa, the rhizome decoction of Polystichum pungens provided a vermifugal enema for intestinal worms.
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This herb was also employed as a wound-healing remedy – the dried fronds being powdered and sprinkled on the injury, a recommendation that is supported by studies that have showing extracts had useful antibacterial activity (Grierson & Afolayan 1999). In Papua New Guinea a Polystichum species was fire-heated and the juice applied to the groin for glandular swellings. Chinese medicine also utilised Polystichum omeiense as a diaphoretic ‘to lower the temperature of the stomach’, while P. fragrans was taken for poisoning or employed as an anti-diarrhoeal agent (Perry & Metzger 1981; Duke & Ayensu 1985; Stopp 1963). Little is known regarding the use of Australian Polystichum ferns – of which there are seven native species. Those found in southeastern Australia include Polystichum australiense, P. fallax, the Broad Shield Fern (P. formosanum) and the Mother Shield Fern (P. proliferum). Polystichum whiteleggei and P. moorei are found only on Lord Howe Island, while P. vestitum is restricted to Macquarie Island. Polystichum fragile (now Revwattsia fragile), is a rare tropical Queensland fern.
was so hard to identify in early investigations. Pterosin B belongs to a group of chemicals (indanones) that were found in Bracken during the 1970s. Related compounds have been found in other plants – for example, toxic illudins in the poisonous North American Jack O’Lantern mushroom (Omphalotus illudens). The National Cancer Institute of the USA took an interest in the evaluation of these compounds and found that the illudins and ptaquiloside had selective toxicity against human myelocytic leukaemia and other carcinoma cells. It was not until the late 1990s that studies ultimately established the chemical basis of Bracken’s activity. Research has continued to evaluate these findings – as well as investigating the antiviral and anti-carcinogenic potential of ptaquiloside and related compounds. There are other areas of potential pharmacological interest. Indeed, an indanone with a structural similarity to the pterosins has been developed as an anti-Alzheimer’s drug and approved for use in the USA and the UK (Bradley 2010; Potter & Baird 2000; Yamada 1998).
Cooking Away Carcinogens? Ptaquiloside Chemistry
Jack O’Lantern Mushroom, Omphalotus illudens. (Courtesy: Walt Sturgeon, CC-by-SA 3.0)
Chemical studies have found that ptaquiloside degraded readily to form pterosin B and D-glucose, which was part of the reason that it
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Interestingly, it was found that some traditional Japanese cooking practices greatly reduced Bracken’s carcinogenic potential – although studies clearly demonstrated that serious attention had to be paid to the type of processing used. In Japan, the starch sourced from the astringent rhizome could be made into a form of miso. The young fronds (warabi or zenmai) were also popular – eaten fresh, salted, sundried or pickled. Fresh fiddleheads were prepared by brief immersion in hot water containing wood ash or sodium bicarbonate to reduce the bitterness. Early experiments showed that preparing the crosiers with wood ash or sodium bicarbonate (alkaline agents) reduced the tumour incidence in animal studies from 78.5 per cent to 25 per cent – although this lowered risk would still be considered too high (Hirono & Yamada 1987; Hirono 1987, 1972). Investigations showed that warabi croziers (young shoots) from the toxic latiusculum variety of Bracken can contain highly variable levels of pure ptaquiloside:
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13–169 kg could be present in 13,000 metric tons that was destined for culinary use. Clearly, even though ptaquiloside should be transformed to its innocuous form (pterosin B) during processing with an alkaline agent, there may still be carcinogenic potential.7 This has been confirmed in studies on rats. In addition, Osmunda japonica fiddlehead, or zenmai. (Courtesy: kropsoq, the wash-water was found to be strongly GFDL, CC-by-SA-2.5) tumorigenic – in other words, inadequate washing and re-cooking (without discarding the used water) would leave residual toxins in the crosiers at potentially toxic levels (AlonsoAmelot & Avendano 2002; Saito 1989b). 7 In addition to the major toxin ptaquiloside, subsequent studies have shown that around 20 different kinds of pterosides and pterosins (the latter being formed via hydrolysis of ptaquilosides) can be present in Bracken. Pterosins do not appear to have the carcinogenic potential of ptaquiloside, although some may have experimental cytotoxic activity (Potter & Baird 2000).
Edible Ferns
Around the same time that Bracken was undergoing close scrutiny, researchers turned their attention to the evaluation of other ferns that were considered to be edible. Those found to be devoid of experimental toxicity included the Cinnamon Fern (Osmunda cinnamonea, syn. Osmundastrum cinnamoneum), Osmunda japonica, the Interrupted Fern (Osmunda claytoniana, syn. Osmundastrum claytonianum), the Hay-scented Fern (Dennstaedtia punctiloba), Matteuccia orientalis (syn. Pentarhizidium orientale) and the Ostrich Fern (Matteuccia struthiopteris). The latter, which is native to Canada and the USA, has been prized as a delicacy and continues to be the primary ingredient of a popular ‘spring tonic’. Nutritionally it appears comparable
Interrupted Fern, Osmunda claytoniana, Quebec. (Courtesy: Jean-Sébastien Girard, CC-by-SA 2.0, Wikimedia Commons)
Royal Fern, Osmunda regalis.
to Asparagus, with a high potassium and low sodium level. However, there is the possibility of allergic reactions in some individuals (Saito 1989; Newberne 1976; Blake 1942). The Royal Fern (Osmunda regalis) has been traditionally utilised in Italy as a remedy for bone disorders (fractures, joint pain) and pain (rheumatism, arthritis) (Molina 2009). However, while this suggests good healing, antiinflammatory and analgesic properties, little evaluation of the herb appears to have been undertaken. The Royal Fern has a useful ability for detecting environmental pollution, making it suitable for use as a biomonitoring agent. It, as well as Confederate Spiderwort (Tradescantia paludosa) and Corn (Zea mays), have been used to measure air quality around cities in America and nuclear
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power plants, as well as near industrial waste sites and sewage sludges. Osmunda has also been used to assess to mutagenic potential of polluted waste waters (Sandhu & Lower 1989; Klekowshi & Levin 1979). There are studies of Osmunda japonica, which is very closely related to the Royal Fern, that have shown that it contains antifeedant compounds against the Yellow Butterfly (Eurema hecabe mandarina), as well as polysaccharides with an inhibitory effect on blood agglutination agents. The latter are used in studies of blood chemistry (Numata 1990; Akiyama 1988).
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Left and above: Dicksonia antarctica.
Ostrich Fern (Matteuccia struthiopteris).
In addition, studies into the carcinogenic potential of fern spores determined that Osmunda regalis spores did not cause DNA damage in vitro – although a number of other species did: Anemia phyllitidis, Dicksonia antarctica, Pteris vittata and Sadleria pallida. The highest level was associated with Bracken (Pteridium aquilinum) spores, although the extent of the damage varied according to the dose and length of exposure. While the importance of this finding to human health has not been determined, it would appear to be linked to Bracken’s carcinogenic potential – although the toxicology of airborne spores remains a matter of conjecture. Certainly, some ferns can produce massive amounts of spores. A single Bracken frond can produce around 300 million spores, and a frond of the Tree Fern, Dicksonia antarctica, 750 million (Siman 2000).
Bracken spore cases. (Courtesy: Equinest, flickr, CCby-SA)
Some other chemical considerations can exert an influence on the toxic potential of Bracken. Simply boiling it does not raise the temperature high enough to remove or inactivate accessory toxins in the plant. Shikimic acid, prunasin and thiaminase are only destroyed at very high temperatures. The cyanogenic glucoside prunasin (which may be present in quite high amounts) can impart a bitter character to the
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fern crosiers – as would their high tannin content (10– 16% tannin and phenolic acids). Among the phenolic components the flavonoids quercetin and rutin are present, and it has been suggested that they may have co-carcinogenic properties with the potential to transform viral papillomas into cancerous lesions in ruminant animals. However, consideration of the substantial health benefits of these flavonoids suggests that they are unlikely to be a hazard for human consumption at normal levels (Latorre 2009; AlonsoAmelot & Avendano 2002).
The Bungwall Fern
The Bungwall Fern is a semi-aquatic species that was another source of Aboriginal food. The first encounter with its use as a food was by three exconvicts named Pamphlet, Finnegan and Parsons, who were stranded at Stradbroke Island in the early 1820s and provided with food by the local Aboriginal people (Colliver & Woolston 1975). Thomas Bancroft (1895) later provided details of its preparation: Blechnum serrulatum is a freshwater swamp fern growing to the height of six feet; it has a wide distribution, not alone in Queensland, but throughout the world. The whole root or rhizome is the part eaten; it is first dug out with a sharpened stick, dried in the sun for a short time, roasted and afterwards bruised, when it is ready to be eaten in conjunction with fish, crabs, and oysters. The Bungwall stone is not unlike a stone tomahawk, the sharp edge being used to bruise the rhizome against a slab of blood wood (Eucalyptus corymbosa, Sm.); wood being used in preference to stone to avoid grit, and likewise a stone in preference to a metal instrument to avoid chips.
Bottles containing oil from Eucalyptus sieberiana, made by the Technological Museum, Sydney, c. 1900–1940. The leaves of the Ironbark, Coast or Silvertop Ash, Eucalyptus sieberi (formerly E. sieberiana), contain shikimic acid – a compound that has been utilised as a starting point for the development of the influenza preventative drug, Tamiflu. (Image courtesy: Powerhouse Museum, Sydney)
Certainly, the extensive preparation techniques employed by New Zealand Maori and Australian Aboriginal people appear to have significantly reduced the toxicity of Bracken frond and root harvests.8 The Aboriginal custom of roasting the fiddleheads in hot ash may have even raised the temperature enough to deactivate the toxins – maintaining it at a high level for a fairly long period without burning the produce. Drying, washing and roasting would have been even more efficient at removing the toxic load. Although occasional use of Bracken was probably not harmful, eating the fern regularly as part of the normal diet would have been decidedly unwise (Crowe 1990; Isaacs 1994). 8 In some places Aboriginal people also utilised the underground stem (below the new shoots), but not the root, for the extraction of a slimy, tasteless form of starch (Low 1992).
The stones were described as being ‘fragments of water-worn pieces of basalt, split by fire into the desired shape. We were fortunate in finding several Bungwall stones and also a Bunya Bunya stone; they were hidden at the butts of large Cypress Pines (Callitris columellaris, F.v.M); in all probability their owners have long been dead’ (Bancroft 1895). In 1836, James Backhouse had tried the preparation and commented that after roasting and beating with a stone on a log of wood to smash up the fibre, ‘In this state it is eaten, without removing the charred surface; its taste is something like that of a waxy potato, but much more gelatinous’ (Backhouse 1843). Other writers mention that it had a nutty flavour and a reputation for being very nutritious. The root, peeled back to the central core, also provided a form of flour that could be made into a type of bread or biscuit. FS Colliver and FP Woolston, who experimented with the foodstuff, provide substantial details of its preparation and palatability:
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Bungwall Fern (Blechnum indicum). In 1770 this plant was collected with Cyclosorus interruptus, another swamp fern, by Joseph Banks and Daniel Solander at Botany Bay. (Courtesy: Peter Woodard)
We discovered firstly that like some other vegetable foods, the rhizomes keep very well; on one occasion some were processed three weeks after collection and found to be perfectly edible. All the rhizome material has long tough fibrous (almost stick-like) strings running longitudinally. These are surrounded by white farinaceous material which is enclosed in a skin from which grows masses of fibrous roots. When the rhizomes were placed in hot ashes these roots burnt off quite easily. We found that if the fire was too hot the whole mass dried quite rapidly and then caught alight and burnt, so that after lightly roasting, the rhizomes could be peeled quite easily. If after peeling the rhizomes are dried by heat, then the whole mass can be easily pounded into a dry meal (using bungwal stones) and eaten. We found the taste biscuit-like and agreeable. On the other hand, if complete dryness of the rhizome is not attained, then the long tough strings, even despite chopping, made the mass difficult to eat. However, the rhizome can still be chewed and the strings spat out. In the only photograph we could find to illustrate the processing of bungwal the aborigines appears to be using a chopper-type tool on a log. We suggest that this was part only of the entire process, having found the rhizomes can be cut or trimmed quite readily in the same manner (using a quartzite chopper from Dunwich). The roasted dried material would then be pounded to meal using the top and bottom bungwal stones. From continued usage, the bottom stones acquired a slightly dished shape whilst the top stones or pounders become somewhat squarish. We suggest that the aborigines had no need to visit the swamps every day, and on occasions they loaded their rush dillies and laid in several days supply, and processed it when the need arose (Colliver & Woolston 1975).
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The Bungwall Fern is prevalent along the New South Wales coast, ranging to southern Queensland; it is also found in the tropics (northern Queensland, Northern Territory and Western Australia). At Tully (northern Queensland), Dr Hugo Flecker (1948) noted that the pounded roots were made into a porridge, while Walter Roth (1901) mentions the use of Blechnum orientale, which is more common in the northern tropics. The fiddleheads of some Blechnum species were also cooked in an earth oven in New Zealand, about which Andrew Crowe comments: ‘they have a mild and slightly slimy taste but are delicious boiled for 15 minutes and dressed with oil, lemon juice, garlic and salt’ (Crowe 1990). Little appears to be known about the medicinal use of these herbs, although Henry Burkill recorded that the Chinese utilised Blechnum orientale for treating urinary tract disorders (Burkill 1935). In Indonesia the fiddlehead was crushed, fire-heated, and applied to the rim of a weeping sore to draw out infection – which probably relates to its similar use in Malaysia as a poultice for boils (Leaman 1991). The young shoot (pounded) was also utilised for boils in China, while Blechnum eberneum was made into a tincture (soaked in wine) and applied as a healing agent for injuries (Perry & Metzger 1981). There is one other more unusual note regarding Blechnum orientale – in Papua New Guinea it was
Blechnum cartilagineum is a widespread species along the eastern coastline – found from Cape York in northern Queensland, and ranging to Victoria and Tasmania.
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used to induce permanent sterility in women. The top leaf of the fern was eaten for three days and then, after a break of two weeks, the process was repeated (Holdsworth & Lacanienta 1981; Holdsworth 1977). In Fijian traditions, Blechnum milnei stem (peeled and pounded with the leaves into a mash) was poulticed on muscular problems – for example, a strained back or the limbs from carrying heavy loads. A leaf decoction was also taken to cure fever after childbirth (Cambie & Ash 1994). There are 24 native species of Blechnum, among them a number of interesting endemic species such as B. articulatum, B. whelanii and B. wurunuran from northern Queensland, B. gregsonii from New South Wales, and B. norfolkianum from Norfolk Island – as well as B. contiguum, B. fullagari, B. geniculatum and B. howeanum from Lord Howe Island.
Toxic Animal Fodder
The toxic effects of Bracken have been known for centuries, giving it a well-deserved reputation as a hazardous animal feed. It can cause serious illness that primarily manifests as a loss of condition with the concurrent development of coordination problems. The amount of Bracken in the diet, and the types of feed with which it was combined, could substantially influence its toxicity. It was known that the thiaminase present in Bracken did not overtly affect ruminants (sheep, cattle) that naturally produce B1 in the gut flora. However, serious incidents of poisoning in cattle and sheep involved acute, as well as cumulative, toxic reactions which were not due to thiaminase. The toxicity was characterised by a crippling depression of bone marrow activity (disappearance of white blood cells and internal bleeding). Few animals recovered from such severe incidents. Other chronic problems included the development of ‘bright blindness’ (associated with retinal degeneration), as well as tumour development in sheep and haematuria (bladder haemorrhage). Ptaquiloside was finally identified as the toxic principle associated with blood abnormalities and various other symptoms (Pakeman & Marrs 1993, Dowling & McKenzie 1993; Saito 1989a, 1989b).
Later investigations provided greater clarification of the situation. One study of the occurrence of bovine enzootic haematuria and/or acute haemorrhagic syndrome in New Zealand cattle showed that the conditions were prevalent where the toxin levels in Bracken were high. The survey involved an evaluation of 275 samples that determined ptaquiloside concentrations varied dramatically: 280–13,300 (mean 3,800) mcg/g (dry-weight basis) in 63 per cent of samples containing the toxin. Interestingly, some entire areas were free of the toxin, with no detectable levels found in Bracken samples (Rasmussen 2008). The types of cancer suffered by cattle with chronic Bracken (Pteridium aquilinum) toxicity has been of interest to researchers due to their similarities to human cancers. Squamous cell carcinomas of the upper digestive tract that resemble human head and neck cancers occur, while carcinomas of the urinary bladder resemble urinary tract carcinoma in humans. The latter condition in cattle has also been linked to infection with bovine papillomavirus (type-4). Ptaquiloside-induced cancer studies were later developed for experimental use in investigating these tumorous conditions (Masuda 2010; Roperto 2010). Studies have also suggested that Pteridium aquilinum has an immunosuppressive effect that may contribute to its carcinogenic activity. For instance, it is possible that poor immune function may be linked to a higher susceptibility to bovine papilloma virus infection, or contribute to the malignant transformation of papilloma cells (Latorre 2009).
A Secret Carcinogen?
The fact that ptaquiloside is highly water soluble may have serious environmental health implications under certain conditions. In 2003 a study by Holm Rasmussen and colleagues, examining the well-water on Danish and Swedish farms that had Bracken growing in the area, made a discovery with horrifying potential. Extremely high levels of ptaquiloside were present in the water – sometimes over 20,000 times higher than the suggested tolerable limits for environmental carcinogens. Although
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Bracken flourishing alongside a body of water. (Courtesy: Brian Harry, NPS.gov)
the full implications remain unclear, this finding may be linked to ‘hot spots’ of gastric and oesophageal cancer in places as diverse as Wales and South America. Measurements of the toxin in soil and soil-water samples taken at different times of year found that after heavy summer rainfalls the ptaquiloside was washed out of the Bracken fronds by rain, and on farms where the watertable was high (5–10 m below ground) the toxin was much more accessible. A comparison of toxin levels in the plant and soil not only showed high levels in the plant fronds – water-based soil solutions appear to have equally problematic potential. While most mains water supplies are unlikely to have a Bracken contaminant, there may be some Bracken-infested regions that have a higher risk factor. The substantial variability in the amount of the carcinogen that is present in the plant will influence the level of exposure – thereby affecting its potential as an environmental carcinogenic hazard. The variation in ptaquiloside levels can be significant (Rasmussen 2005, 2003): frond: 213–2145 mcg/g rhizome: 11–902 mcg/g soil material: 0.22–8.49 mcg/g soil solution: 200–8500 mcg/litre
In addition, soil type was found to be an important consideration: peat (acid) and chalk (alkaline) helped to degrade the carcinogen. Slightly acidic sandy soils (pH 5–6) in cold climates showed
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the highest risk of retaining the compound intact. The activity of soil microorganisms also influenced the biodegradability of ptaquiloside (Ovesen 2008; Engel 2007; Alaya-Luis 2006; Schmidt 2005; Ravilious 2004). Equally concerning is the fact that important agricultural crops such as canola and clover, which are often planted on sandy soils with a high watertable, yield toxins with structures similar to that of ptaquiloside. Although these toxins have not shown carcinogenic activity, it is possible that they can have similar potential for soil accumulation. However, there may be even more trouble ahead. The development of GM crops with an increased natural defence against pests and weeds means that these crops carry genes that code for a high production of toxic compounds that could act in a similar manner to the ptaquiloside carcinogen (Ravilious 2004; Rasmussen 2003).
A Medicinal Reputation
Medicinally, Bracken has long held a reputation as a useful anti-diarrhoeal and vermifugal agent in numerous countries. It has been employed since ancient times as an anthelmintic. As Bracken contains tannin, which is astringent, its anti-diarrhoeal effects are probably associated with this compound. The herbalist Nicolas Culpeper recorded its traditional use: ‘The roots being bruised and boiled in mead and honeyed water, and drunk kills both the broad and long worms in the body, and abates the swelling and hardness of the spleen. The leaves eaten, purge the belly and expel choleric and waterish humours that trouble the stomach. The roots bruised and boiled in oil or hog’s grease make a very profitable ointment to heal the wounds or pricks gotten in the flesh. The powder of them used in foul ulcers causes their speedier healing’ (quoted in Grieve 1931). The leaves contained a tapeworm-killing saponin (pteridin9). Indeed, it appears possible that the use of Bracken as a regular part of the diet did reduce the incidence of intestinal worms. In Africa it was used as a worm-remedy in animals, while Australian 9 Pteridine [sic] has been listed as a taenifuge (Duke & Ayensu 1985).
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The frontispiece from Culpeper’s Herbal, 1814, and a purging ointment recipe incorporating Male Fern.
country areas bushmen have employed decoctions of the fern for ridding animals of ticks (Hiddins 2001; Lassak & McCarthy 1992; Roberts 1990). In Australia the juicy young stem was applied externally by Aboriginal people for treating insect bites and stings. Similar uses of the juice have been reported in Africa, where it was also applied to veld sores and rashes (Webb 1948, Cribb & Cribb 1981). However, one of the more unusual recommendations for the herb has been recorded in Papua New Guinea – where Bracken fronds and Nothofagus grandis leaves were eaten with fish when a person ‘feels sick from the smell of decay at a funeral’ – suggesting an anti-nausea effect. (Holdsworth & Sakulas 1992) It is extremely interesting to find that Bracken earned a rather unusual reputation as a remedy in New Zealand during the influenza epidemic of 1918–19. A decoction of the plant was regarded as being ‘remarkably effective’. Additionally, the burnt
frond ash was applied to severe burns, while the small tender shoots were chewed to treat dysentery. It is worth noting that Bracken’s antimicrobial properties have been attributed to the phenolic acids present in the fronds.10 These compounds, which are used by the plant for defence, have demonstrated both antifungal and antibacterial activity, although their concentration can alter seasonally. Mixtures of phenolic acids can have a synergistic effect that suggests they are more effective in combination – thus the natural product can have advantages over isolated chemicals (Crowe 1990; Booker 1987; San Francisco & Cooper-Driver 1984). Pterosins from Pteris inequalis have also shown antibacterial activity against Bacillus subtilis (Kobayashi 1975).
10 Phenolics not only protect against plant pathogens, they have a deterrent activity against pests such as locusts.
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Table 9.1 Bracken as a medicament Country
Europe
Italy
USA – American Indian
Listing and medicinal use (reference) It should be noted that since Bracken has fallen from favour due to its toxicity, its medicinal use is no longer regarded as being important and tends not to be recorded in the literature. Therefore, as the plant gradually fades into obscurity, this knowledge is being lost. Bracken (Pteris aquilina) (Culpeper 1653): • Roots (decocted with mead and honey water) utilised as a vermifuge, for swelling and hardness of the spleen. • Leaves eaten as a purge. • Root ointment: for wound healing purposes and foul ulcers. Pteridium aquilinum (Guarrera 1999)L • Insect repellent: bundles of fronds hung in windows or rooms to remove flies; leaves also rubbed on skin as a repellent. • Investigations of Bracken’s mosquito larvicidal properties have been undertaken in Bangkok (Nitcharat 2001). Cherokee medicine (Bracken; Moerman 1986): • Root: anti-emetic, tonic, antiseptic, given for ‘cholera morbus’. • Root: decoction hair rinse or roots rubbed on scalp to encourage hair growth. Iroquois medicine (Brake): • Brake root decoction taken following birth and for diarrhoea. • Brake compound decoction: taken for rheumatism; for ‘weak blood’; uterine prolapse; urine retention in men; early stages of consumption (tuberculosis); infection (probably venereal disease). • Brake: taken for menstrual problems; liver and rheumatism medicine. Koasati remedy (Common Bracken): • Ground roots for chest pain. Menominee (Pteris aquilina): • Root decoction for ‘caked breast’. Micmac (Pteris aquilina): • Plant frond tonic for weak babies and old people. Ojibwa (Pteris aquilina): • Root infusion to allay stomach cramps in women; smoke from dried leaves to relieve headache. Yana (Pteris aquilina): • Roots: heated AND pounded to make poultice applied to burns.
South America (tropics)
Pteridium aquilinum • Tropics: utilised as a hernia remedy (Levi-Strauss 1952). • Ecuador: rhizome used as diuretic and to treat chest complaints. P. arachnoidea and P. esculentum were utilised in the same manner (Varea 1922).
India
Pteridium aquilinum (= Pteris aquilina; Chopra 1956): • Rhizome: astringent, anthelmintic. • Frond and rhizome decoction: given in ‘chronic disorders arising from obstructions of the viscera and spleen’. Pteridium aquilinum (Bracken; Duke & Ayensu 1986): • Stem: young shoot diuretic, refrigerant, vermifuge, used for rectal prolapsed. • Root: tincture in wine for rheumatism. • Rhizome: starch used medicinally. • Juice: antibacterial (Gram-positive bacteria). • Stem and young shoots (combined): purgative for expelling intestinal worms. Pteridium aquilinum (= Pteris aquilina, P. esculenta; Perry & Metzger 1981): • Roasted and powdered roots mixed with sesame oil: used to treat snake bite. • Root decoction: diuretic and sedative, supposed to activate blood circulation.
China
Southeast Asia (IndoChina) Thailand
Pteridium aquilinum (Anderson 1986): • Lahu people: crushed fronds used as antiseptic and astringent agent • Akta people: pounded rhizomes with powdered Selaginella helferi leaves applied to snake bite.
Papua New Guinea
Pteridium aquilinum (Perry & Metzger 1981): • Juice: used as a stimulant. • Young leaves: can cause mild indigestion. Pteridium aquilinum (Powell 1976): • Mt Hagen: the petiole sap of the common bracken is used to treat toothache and mouth infections. • The Highlands Chimbu use this plant in magic and ritual ceremonies.
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A Toxic Anthelmintic
Shaggy Shield Fern (Dryopteris atrata). The Dryopteris genus has been found widely distributed around the globe – Europe, Asia, India and Africa – also ranging from temperate America to the Andes of South America.
There are only a few Dryopteris species found in Australia. Dryopteris cycadina (often known as D. atrata in the horticultural trade) is naturalised in a few places in Victoria. The Queensland native species are Dryopteris hasseltii and D. sparsa – the latter is considered rare as it is only found at Mt Bartle Frere in northern Queensland. However, both species have a more widespread overseas distribution (New Guinea, the Philippines, Pacific Islands, Malaysia, India, Southeast Asia and China). A number of native species that were originally thought to be Dryopteris were subsequently classified in the genera Ampelopteris, Christella, Coveniella, Hypolepis, Macrothelypteris and Pneumatopteris. The Male Fern (Dryopteris filix-mas) has an ancient medicinal reputation. Its vermifugal effects were known in ancient Rome and Greece – this use of the fern being mentioned in the works of numerous great physicians such as Dioscorides, Theophrastus, Galen and Pliny. The seventeenth-century herbalist John Gerard commented: ‘The roots of the Male Fern, being taken in the weight of half an ounce,
driveth forth long flat worms, as Dioscorides writeth, being drunke in mede or honied water, and more effectually if it be given with two scruples, or two third parts of a dram of scammonie, or of black hellebore; they that will use it, must first eat garlicke’ (quoted in Grieve 1931). Over time the use of the herb lapsed – until revived in 1869 by a French medic named Jobert. Oil prepared from the rhizome (a dark green viscous liquid which effectively extracted the active constituents of the herb) gave excellent results. The Martindale & Westcott Extra Pharmacopoeia of 1928 included the following details: Filicin: prepared by triturating the ethereal extract of Filix Mas [Male Fern] with 10 times its weight of Magnesia. The liquid is filtered off and rejected. The Magnesia compound is treated with water and filtered and Hydrochloric Acid added to this: the resulting precipitate, which is dissolved in Ether and then dried, is ‘Filicin’ … Given by mouth in large doses, it causes vomiting and diarrhoea. It is eliminated by the bile. An investigation on flat-worms and tape-worms showed it to be an excellent helminthicide: the ingested Filicin reaches the intestine, impregnates the taenia, passes into the blood and then into the bile and returns to the intestine, where it again acts on the parasites - this cycle being repeated many times … There are no toxic effects if given in suitable doses. Taenia are stated to be expelled in a few hours. Combined with Calomel, both an anthelmintic and purgative action is obtained.
The fact that it was not considered toxic ‘in suitable doses’ is very interesting in light of its toxicological potential. Maude Grieve provided further details of filicin’s use: ‘The liquid extract is one of the best anthelmintics against tapeworm, which it kills and expels. It is usual to administer this worm medicine last thing at night, after several hours of fasting, and to give a purgative, such as castor oil, first thing in the morning. A single sufficient dose will often cure at once. The powder, or the fluid extract, may be taken, but the ethereal extract, or oleoresin, if given in pill form is the more pleasant way of taking it.’ The British Pharmaceutical Codex (BPC) of 1949 differed in its recommendations: ‘For two days before the extract is administered the patient should be put on a low-residue diet and given a saline purgative each night … Since absorption of extract of male
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Dryopteris filix-mas, from Bilder ur Nordens Flora, CAM Lindman, 1917. Male Fern rhizome required preparation before use. It was cleaned, removing the scales and side roots, to leave only the lower swollen portion, which was sliced in half and dried before use. Maude Grieve (1931) noted: ‘For pharmaceutical use, it is reduced to a coarse powder and at once exhausted with ether. Extract obtained in this way is more efficacious than that which has been obtained from the rhizome that has been kept for some time. It should never be more than a year old.’
fern may be increased by the presence of fat in the intestine, fatty meals and oils such as castor oil should not be given.’ Although it was originally thought that filicin was rarely found outside the genus Dryopteris, later studies showed that many ferns can contain substantial amounts. One review of eighteen Indian ferns determined that fifteen contained levels of 1.5 per cent or more. A number of other European ferns contained equivalent amounts, as did the American species Dryopteris marginalis (Evans 1989).
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Male Fern Extract, from the British Pharmacopoeia, 1914. By 1949 the British Pharmaceutical Codex required not less than 1.5 per cent filicin in the crude drug and 21–23 per cent oleoresin. This compound was present in the hair-like scales on the rhizome and the frond bases.
Unfortunately, despite its exceptional efficacy, Male Fern was highly toxic. In addition to an irritant effect on the gastrointestinal tract, its use could result in muscular weakness and visual disturbances. The following dangers were noted in the Martindale & Westcott Extra Pharmacopoeia of 1928: ‘Moderate doses almost invariably produce bilirubinaemia and in large doses jaundice. There is risk of chronic cirrhosis of the liver developing.’ About 100 cases of serious visual impairment were also reported around this time, mainly in South Germany and Switzerland. The BPC of 1949 included the following additional observations: ‘It is contraindicated in anaemia and pregnancy and in old people and infants. Toxic effects are rare and are manifested by headache, nausea, vomiting, severe abdominal cramp, diarrhoea, albuminuria [protein
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Dryopteris filix-mas and Asplenium filix-femina, from Gerard Dewes, A Newe Herball or Historie of Plantes, 1578. (Left) The Lady Fern (Asplenium filix-femina) was noted to have properties similar to the Male Fern, although having a somewhat less powerful effect. (Right) The Prickly-toothed Shield Fern (Aspidium spinulosum) provided another Male Fern substitute.
POISONOUS PTERIDOPHYTA
in the urine] and dyspnoea [difficulty breathing]. In severe cases, convulsions, loss of reflexes, optic neuritis, leading to temporary or permanent blindness, may occur. Death sometimes ensues from respiratory or cardiac failure.’ Obviously this was not plant to fool with. Male Fern had a few other useful attributes, which Nicolas Culpeper noted: ‘The roots bruised and boiled in oil or hog’s lard, make a very profitable ointment to heal wounds. The powder used in foul ulcers, drieth up their malignant moisture, and causeth their speedier healing. Fern being burned, the smoke driveth away serpents, gnats, and other noisome creatures, which in fenny countries, in the night time, molest people lying in bed with their faces uncovered. It causeth barrenness’. The Wood Fern (Dryopteris dilatata) was also used as a wound remedy by the American Indians – the pounded roots applied directly to cuts (Lloyd 1964), with similar applications being recorded from the West Indies (May 1978). While Dryopteris filix-mas is the best known and most widespread of the Dryopteris, there are other
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species within the genus that have had limited medicinal value. No doubt the therapeutic use of alternative ferns as vermifuges reflected a similarity in their chemical components. In Africa, Dryopteris athamantica (syns Aspidium athamaniticum, Lastrea athamantica) was a Zulu vermifuge which was regarded as being as effective as Male Fern for tapeworm – if not more so. Dryopteris inequalis was another anthelmintic agent used by the Zulu and Xhosa (Watt & Breyer-Brandwijk 1962). Multitudinous additional species have been utilised for this purpose across the world: Dryopteris parallelogramma and D. palaceae (Colombia), D. ampla (West Indies), D. parasitica (Ivory Coast, Africa), D. crassirhizoma and D. sophoroides (China), Polypodium polypodioides (USA), P. suspensum (West Indies), P. crassifolium (Ecuador), P. percussum (Ecuador), Pteris dentata (Africa), Aspidium falcatum (China) and A. polymorphum (India) (Riley 1994). Other species that have been listed as useful vermifuges illustrate the variety of ferns utilised in different countries, and the variation in plantparts considered suitable for use (Jones 1987):
Male Fern, with new fronds and spore cases. Mature Ferns produce spores on the underside of their leaves in spore cases (sporangia), and it is the characteristics of these structures that help identify many species. The spores within are tiny, having the appearance of coloured powder (black, brown, reddish, yellow or green). They are the beginning of the fern’s complex reproduction strategy, growing into tiny plantlets (a prothallus or gametophyte) given the right environmental conditions. This gametophyte usually (but not always) requires fertilisation to develop into an adult plant. This is not the only method of propagation. For instance, Bracken can also grow by spreading rhizomes, while other plants sprout baby ferns on the
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons Taenia solium, the Pork Tapeworm, can infect pigs and humans. From Die Cephalopoden, 1910, Carl Chun.
• E urope and Mexico: Lycopodium selago (spores). • China: Acrostichum aureum (rhizomes). • South Africa: Asplenium adiantum-nigrum, Cyathea mannjana and Dryopteris anthelmentica (fronds). • Africa: Asplenium furcatum (rhizome). • USA: Asplenium ruta-muraria (rhizomes); Dryopteris cristata (fronds), Pellaea atropurpurea (all parts). • India: Blechnum orientale, Drynaria quercifolia, Dryopteris barbigera, D. blandfordii and D. schimperiana (rhizomes). • Europe: Dryopteris carthusiana, Pteridium aquilinum (rhizomes). • Canada: Dryopteris parallelogramma (rhizomes).
A Traditional Chinese Anthelmintic In Chinese medicine the fern Dryopteris crassirhizoma has been used to prepare the drug Guan Zhong (specifically Dong Bei Guan Zhong).11 The rhizome was not only useful for tapeworm, as it had a good reputation against numerous other intestinal parasites (hookworm, pinworm, roundworm), as well as liver-fluke in animals. Its use was necessarily combined with 11 A number of additional ferns have been utilised for the preparation of Guan Zhong. They included Lunathyrium acrostichioides, Matteuccia struthiopteris, Osmunda japonica, Blechnum orientale, Brainia insignis, Cyrtomium fortunei and Woodwardia japonica.
bioavailability of the toxin filmarone is of interest as it is not absorbed unless taken with fatty foods – a combination to be avoided as it could cause gastrointestinal upsets (vomiting, diarrhoea), visual disturbances and muscle paralysis Dryopteris crassirhizoma. (Courtesy: Dalgial CC-by- (striated muscles). Guan Zhong has SA 3.0 Wikipedia) had a good medicinal reputation as a potent haemostatic useful for treating conditions such as haemoptysis (spitting blood), nose bleeds (epistaxis) and bloody stools. Intramuscular injections of the herb have been used clinically in uterine bleeding (postpartum bleeding, following miscarriage, or in bleeding after surgery). There were no side-effects and the treatment was reported extremely effective in most cases (91% successful). The herb also possessed analgesic and anti-inflammatory activity. Experimentally it was shown to increase uterine contractions and tension, and its use was therefore contraindicated in pregnant women – nor was it recommended for children, weakened individuals, or in cases of gastrointestinal ulceration (Bensky & Gamble 1986; Yeung 1985). In addition, the herb was regarded as being a good remedy for skin problems characterised by ‘heat’ and toxin accumulation – for example, sores, carbuncles, measles and mumps – as well as being a useful febrifuge for treating influenza, meningitis and pneumonia. Trials of its use as a preventative for influenza epidemics determined that the remedy had antiviral and antimicrobial properties. Clinically it reduced the incidence of influenza by about 20 per cent – while 33 per cent of the control group caught influenza, it affected only 12 per cent of those undergoing treatment (Bensky & Gamble 1986; Yeung 1985). Recent investigations have shown extracts had antibacterial activity against MRSA (methicillinresistant Staphylococcus aureus) (Kwon 2007).
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This activity appears to be associated with flavaspidic acids (phloroglucinols12). These have shown potent antioxidant properties, with good activity against Gram-positive bacteria – although they did not demonstrate activity against fungi or Chlorella (blue-green algae) (Lee 2009, 2003). Rhizome extracts were shown to contain triterpenes with strong anti-HIV activity, notably dryopteric acids and ursolic acids – as well as kaempferol derivatives (Lee 2008; Min 2001). Studies on the antiviral effects of other ferns have shown interesting positive results, notably Polypodium aureum, P. vulgare, P. glycyrrhiza and Dryopteris filix-mas. Polypodium glycyrrhiza attracted additional interest as it contained an intensely sweet constituent (polypodoside A) – around 600 times sweeter than a standard sucrose solution (Kim 1988). Anther fern with antiviral potential is Selaginella sinensis, which contains an antiviral compound (armentoflavone) that is present in other species of this genus. Icelandic Moss (Cetraria islandica) has shown experimental anti-HIV activity (Ma 2001; McCutcheon 1995; Pengsuparp 1995; Husson 1986). Extracts of Osmunda japonica (aerial parts) have also shown potent anti-herpetic (anti-HSV) activity (Woo 1997). Interestingly, investigations of phloroglucinol components from Dryopteris fern extracts have shown anticancer and antiparasitic properties. Studies into the anticancer potential of Guan Zhong extracts indicated good activity against prostate cancer cells (Chang 2010). Screening studies evaluating phlorophenone derivatives from Dryopteris ferns as cancer chemopreventive agents found aspidin, desaspidin, and albicanol had significant inhibitory effects in skin carcinogenesis studies (Kapadia 1996; Na 2006; Ito 2000). Some of these compounds have also shown ichthyotoxic, anti-schistosomal and molluscicidal activity (Socolsky 2011; Magalhães 2010; Ito 2000). 12 Phloroglucinols (acylphloroglucinols) have been found in other ferns, e.g. Dryopteris arguta, and tannin derivatives (phlorotannins) are present in some seaweeds, including Australian species of Zonaria (Wollenweberc 1998; Blackman 1988). Phloroglucinol (benzenetriol) and its derivatives are of interest for use in the synthesis of pharmaceutical drugs. Recent evaluations have confirmed its usefulness as an antispasmodic for veterinary use, particularly for urinary tract disorders (EMEA 2009). Phloroglucinol can also be used for the manufacture of explosives.
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• The Fern family (Pteridophyta) clearly illustrates the poisonous potential of ancient plant lineages, although only a few achieved a limited therapeutic reputation. Ferns often remain an unappreciated aspect of our environment – small herbs of undistinguished character found clinging to existence in nooks and crannies within the urban environment. More valued
The Bird’s Nest Fern (Asplenium nidus) is an attractive native fern that is widely planted as an ornamental. This fern has been utilised in Indonesia as a hair shampoo, the leaves minced and mixed with grated coconut (Hirschhorn 1983). In Malaysia, a cooling lotion made from the leaves (macerated in water) was applied to the head for feverish conditions. A similar preparation also had a reputation for being useful, applied locally, to ease labour pains (Perry & Metzger 1981). In Vanuatu its use as a contraceptive is particularly intriguing – the young coiled frond eaten just following the menstrual period (Bourdy 1996). The latter recommendation suggests that this fern is likely to have other traditional medicinal uses, about which very little is known. It is a fairly widespread species that ranges from northern New South Wales and tropical Queensland to Southeast Asia and the Pacific Islands, India, and eastern Africa.
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are a few species considered to be of great ornamental beauty, such as the tropical Bird’s Nest Ferns (Asplenium nidus and A. australasicum), the Maidenhair (Adiantum capillus-veneris and related species), the Tree Ferns (Cyathea spp.) and the Giant Elephant Fern (Angiopteris evecta). However, the great diversity of these plants and the difficulty in their identification has ensured that there are numerous species about which we still know very little – and even less about their toxic and medicinal potential. They remain an intriguing, and quite under-valued, aspect of our world’s flora that often have interesting environmental roles. Equally interesting are the Cycads – another ancient and intriguing category of plants that has survived since the time of the dinosaurs. Many species have an architectural quality to their shape and form that can make them an outstanding feature in garden plantings, and some have been transported widely around the world by avid plant collectors. Botanic gardens around the globe prize these plants both for the great individuality and uniqueness of the various species and for the fact that many are now rare remnants of a floral past that is slowly being consigned to extinction due to deforestation, extensive urbanisation and industrialisation. Cycads have seen the ages come and go, and they have developed some rather interesting survival strategies over the millennia. A number have been utilised as starch resources – although some had poisonous qualities that required the use of extensive processing. However, it has been their hidden toxicological properties that were to come as a surprise to the medical and chemical professions, and these have been the subject of heated debate that continues to this day.
Asplenium australasicum looks very similar to A. nidus, though the leaf midrib is not as prominent. The plant has a similar range along the east coast – extending to Papua New Guinea, Southeast Asia and the Pacific Islands.
Chapter 10
CYCADS: PREHISTORIC SURVIVORS
A fossil specimen of the Upper Jurassic (Kimmeridgian stage) Cycad species Zamites feneonis. Cycad fossil records date back to the Early Permian period, 280 million years ago (mya), although this group of plants may be older, from the late Carboniferous period (300–325 mya). In evolutionary terms, their exact ancestors remain a mystery, as does their relationship to the development of other plants. (Image courtesy: Heiko Sonntag, Wikipedia, CC-by-3.0)
Cycads are a unique classification, ancient remnants surviving the rigours of Earth’s evolutionary past. Classified as Gymnosperms, they are regarded as an intermediate stage in plant evolution – providing a link between ferns (Pteridophytes) and flowering plants (Angiosperms). The eloquent words of Knut Norstog (2003) explain their importance: ‘I have sometimes used the analogy of the Rosetta Stone for the fund of information stored within the cycads and its importance to the interpretation of plant biology. [The] discovery [of the stone] made it possible to decipher Ancient Egyptian writing and revealed many aspects of this great culture that were previously 349
Cycas media is primarily a Queensland species, ranging along the coastline from the New South Wales border to the tropics – although it is more sparsely found in the Northern Territory and the north of Western Australia.
unknown. In a similar way, the ancient structures and developmental pathways of cycads enable us to make connections between the early origins of seed plants and their present-day counterparts.’ The time-span involved in the evolution of Cycad lineages is impressive. Originating in the Early Permian period, about 280 million years ago (mya), Cycads once dominated the flora during the Jurassic and early Cretaceous periods (208–146 mya). The Jurassic
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was the time of dinosaurs, when warm humid conditions prevailed over much of the globe. It was an era of luxuriant Cycad diversity. Later, the more of changing climatic
conditions, and the Cycads were forced to retreat, in ever diminishing numbers, into shrinking habitats.
Cycad world distribution. The majority of Cycads are Gondwanic in origin and the term ‘Old World’ is often used to describe their ancestry.1 Today, these Cycad lineages are located in the Indo-Australian area and Africa. Tracing their ancestry has proved to be a complex and intriguing undertaking for botanists. In the last couple of decades there has been a resurgence of interest in the botanical importance of the lineages of endemic Cycad genera in Australia (Bowenia, Lepidozamia and Macrozamia) and Africa (Stangeria, Encephalartos) (Norstog & Nicholls 1997). (Courtesy: Tato Grasso, Palermo)
Cycad sign from Flecker Botanic Gardens, Cairns, north Queensland. 1 The ancient continental landmass, known as Pangaea, gave rise to two supercontinents: Gondwana and Laurasia. The differentiation of the world’s flora was subsequently linked to divergences that resulted from this continental separation and the accompanying climatic changes.
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Table 10.1 Worldwide distribution of Cycads
Botanically speaking, the Cycas genus is unique in that it appears to be devoid of any close affinities with the other members of the Cycadales. Cycas is the most widely distributed Cycad family, and the species most important for medical and toxicological research are Cycas circinalis and C. revoluta. Zamia, which is ranked second as far as worldwide distribution is concerned, contains the greatest diversity of species. The closely related Macrozamia is a relatively large genus that is confined to Australia. (For further details see the Cycad pages of plantnet.rbgsyd. nsw.gov.au.) Genus (number of species)
Distribution
Bowenia (2) Ceratozamia (16-18) Chigua (2) Cycas (95) (31 in Australia)
Australia (Queensland) Central America: mainly Mexico; C. robusta extends to Guatemala, Belize C. restrepoi, C. bernalii: South America (Colombia) Southeast Asia, southern China to Malaysia and Indonesia, Japan and Mariana Islands, tropical Australia, Papua New Guinea, western Pacific Islands East Africa and Madagascar: C. thouarsii only Central America: Mexico, Honduras, Nicaragua Central and southern Africa Australia (Queensland, New South Wales) Australia (some species remain unclassified) M. calcoma: Cuba S. eriops: South Africa North America (southern states), Caribbean Islands, Central and South America
Dioon (11) Encephalartos (62) Lepidozamia (2) Macrozamia (42) Microcycas (1) Stangeria (1) Zamia (50–60)
Unique Australian Cycads
Today only remnants of the Cycad family’s former glory are found in tropical and subtropical environments. Over 320 million years ago, the origin of seed plants was one of the most significant events in the evolution of terrestrial vegetation. This allowed the colonisation of habitats to which spore-producing plants were unsuited. The forests of northern Queensland are important in an evolutionary sense as they are home to three Cycad families – the Stangeriaceae (genus: Bowenia), the Zamiaceae (genus: Lepidozamia) and the Cycadaceae (genus: Cycas). There were only a few Cycads that made the drastic modifications enabling them to survive in more temperate regions, notably the genus Macrozamia. Australia has a great diversity of native Cycads – comprising around 25 per cent of the world’s Cycad flora. Many species are limited to restricted locations. The four native genera have very different distribution patterns. Species within the same genus are rarely found in the same area, with different species usually taking over at different sites (although there are exceptions). Of particular importance for Cycad diversity are the Cape York Peninsula, the northern part of the Northern Territory, and the QueenslandNew South Wales border (Hill 2003).
Australia’s northern tropics remain home to a number of unique plants, among them three Cycad families, that trace their ancestry through gymnosperm lineages. Cycas media is a member of one of these families, the Cycadaceae.
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It may come as a surprise to find that an accurate accounting of Cycad diversity has been a problematic exercise in many countries and Australia has been no exception. The first herbarium collections of most native species have been made only since the late 1980s. Botanical research in this area has encountered serious practical obstacles – a situation compounded by the clearing practices on farming lands, which have not only removed entire populations of Burrawang (Macrozamia communis) but also M. moorei, M. pauli-guilielmi, M. lomandroides, Cycas media, C. ophiolitica, C. canalis and C. armstrongii. A number are now listed as species of conservation concern (see Table 10.2) (Hill 2003). Unfortunately many species continue to face severe habitat disruption. This, plus substantial illegal collection will, arguably, lead to irreparable damage to their viability in the wild. The souveniring of wild plants, even in protected areas such as National Parks, has been extremely difficult to police. Dwindling native floral stocks have a direct and significant influence on the environment that may not be apparent in the short term. In particular, the viability of the survival of the many slower-growing Cycad species is easily compromised.
Cycas tuckeri is one of Australia’s rarest Cycads. It is a bluegrey foliaged species that is only found in a single population near Coen, in the far north of the Cape York Peninsula. (Images courtesy: PI Forster, Queensland Herbarium).
MacDonnell Ranges Cycad, Macrozamia macdonnellii, at Cycad Gorge, Finke National Park, Northern Territory. Macrozamia macdonnellii is classified as a ‘Vulnerable’ species and is found only around the MacDonnell Ranges near Alice Springs in Central Australia. Illegal seed collection and habitat disruption due to fire exposure are potential threats to the survival of this species. Seed production is very irregular, with a Cycas angulata (left) and C. calcicola (above) are Northern short period of viability. (Image courtesy: C. Goodwin, Territory cycads that are found around Darwin. Wikimedia Commons)
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Table 10.2 Major Australian Cycad species: location and conservation status Genus: distribution Bowenia Queensland Cycas Queensland**
Cycas Queensland/Northern Territory Cycas Northern Territory (Darwin and nearby regions) Cycas Northern Territory/ Western Australia (northern region) Cycas Western Australia (north) Lepidozamia Queensland
Species and conservation status (E = endangered; V = vulnerable) B. spectabilis (north), B. serrulata (central) C. badensis*, C. cairnsiana(V), C. couttsiana*, C. candida, C. cupida, C. desolata*, C. megacarpa (E), C. ophiolitica (E), C. platyphylla (V), C. scratchleyana, C. semota*, C. silvestris (V), C. tuckeri*, C. xiphiolepis, C. yorkiana* C. angulata, C. brunnea*, C. media (extending to north Western Australia) C. arenicola*, C. arnhemica, C. armstrongii, C. canalis*, C. conferta (V), C. calcicola, C. orientis C. maconochiei, C. pruinosa C. basaltica, C. furfuracea, C. lane-poolei L. hopei (northern Qld)
Lepidozamia Queensland/NSW
L. peroffskyana (southern Qld and northern NSW)
Macrozamia Northern Territory (Alice Springs) Macrozamia Queensland
M. macdonnellii (MacDonnell Ranges) (V)
Macrozamia Queensland/NSW (border) Macrozamia New South Wales
Macrozamia Western Australia (south)
Central: M. miquelii (coastal, ranging south), M. moorei (inland), M. platyrhachis (inland: E), M. serpentina (coastal) Southeast: M. cardiacensis, M. crassifolia (V), M. douglasii, M. longispina, M. lomandroides (E), M. lucida, M. macleayi (single collection from NSW in 1861), M. mountperriensis, M. parcifolia (V), M. pauli-guilielmi (E) South (inland): M. conferta (V), M. fearnsidei (V), M. machinii M. cranei (E), M. occidua (V), M. plurinervia (V), M. viridis* M. communis, M. concinna, M. diplomera, M. elegans*, M. fawcettii, M. flexuosa*, M. glaucophylla, M. heteromera, M. humilis*, M. johnsonii, M. montana, M. polymorpha, M. reducta, M. secunda*, M. spiralis*, M. stenomera M. dyeri, M. fraseri, M. riedlei
* Hill (2003) lists these species as rating various levels of conservation concern – as well as specifying C. canalis subsp. canalis (although this subspecies and subsp. carinata are no longer specified as such, and are considered to be synonyms of C. canalis). ** In 1895 Cycas rumphii was reported from mainland Australia, although this was an error; C. rumphii subsp. normanbyana and C. rumphii f. papuana = C. media subsp. media. Cycas thouarsii and C. circinalis have also been included under C. rumphii, although these species are not found in Australia. In addition, a species on Christmas Island was thought to be C. rumphii, but is possibly C. edentata. This requires botanical clarification.
Strategies for Survival: Insects and Cycads The pollination strategies of the ancient Cycads involved a dependence on insect vectors, representing the earliest examples of insect–plant symbiosis. In Australia, the Cretaceous period over 208–146 mya had a thriving abundance of insect species whose survival and subsequent evolution was intimately linked to the flora of the period. Cycads provided a home for
many of these small denizens. Over time, as their descendants evolved, a few selectively formed intimate relationships with their host plants – relationships that have survived into modern times. Fossils provide tantalising hints regarding this aspect of plant history. In The Greening of Gondwana (1986), Mary E White explains: ‘The Koonwarrra Fish beds of Victoria have a
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rich Insect fauna comprising mainly aquatic Nymphs and some Water Beetles. The Beetles were particularly numerous and probably paralleled the modern situation by having a great deal of interaction with Cycads. Burrawang Cycads, for example, have many species of Weevils always present in their cones. The Weevils lay their eggs in the soft scales of immature female cones and eat the spores of male cones. Their significance as pollinators has been realised only recently as their activities are nocturnal and had not been observed.’ In other species, weevils set up house in the male cones and are chemically deterred from damaging the female seeds. Establishing camp in the male cone ensures that both the insects and their larvae experience less exposure to toxins, primarily cycasin, macrozamin and BMAA (that is, β-N-methylamino-L-alanine). Cycad seeds represent an important stage in the sexual development of plants. Cycads are dioecious – that is, there are separate male (pollen-producing) and female (ovuleproducing) plants. Cycads can therefore produce fertilised seeds only on the female parent, and cleverly utilise insects to move Lepidozamia peroffskyana seeds, showing attachment within the cone the pollen to the female plant cone. Because (Images courtesy: J Brew) Cycads grow above ground level they also represent the development of a structure that is male cones elongate and shed pollen, after which they stronger than the ancient ferns or mosses. Male cones, quickly decay and die. In contrast, the female cones although usually smaller than female cones, can be increase in size and can reach a substantial weight. Indeed, more abundant and more frequently produced on a the seed-bearing cones of Lepidozamia peroffskyana, single plant. The cone scales are modified leaves. In which can be quite massive (weighing up to 38 kg), are female cones, ovules are found near the base. Mature the largest of any gymnosperm (Hall 2004).
Cycad Sex Strategies Cycads have an interesting method of increasing their chances of successful procreation. Strategies that involve insect fertilisation bring with it the associated problem of ensuring that the right insect visits at the right time of the reproduction cycle (Martin 1999). Australian Macrozamia Cycads employ thrips (genus: Cycadothrips) for pollination. The system is mediated by
temperature changes and volatile aromatics that act as repellents and attractants, depending on the plant’s requirements. By these means pollenladen thrips are persuaded to make a mass exodus from their permanent residence in the male plant and undertake a delivery trip to the female plant. The system, however, needs to maximise pollen delivery for a time when the female ovules are
CYCADS: PREHISTORIC SURVIVORS
Cycas media, male cone.
receptive – and, for a short period, the female emits an enticing aroma that is usually utilised by the male cycad. The volatile attractant is composed of β-myrcene (low levels) and small amounts of ocimenes (allo-ocimene and (E)-β-ocimene). Detail of male cone. The thrips then need to avoid the toxic levels of β-myrcene that occur after pollination (when levels rise significantly), and they quickly move to another site on the female cone or back to the male plant after the job is done (Terry 2007). This chemical complexity is a remarkably intriguing aromatic strategy for pollination.
Lepidozamia peroffskyana: weathered male cone, showing characteristic spiral split along the mature cone, when they distend (growing substantially longer) before emitting pollen.
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Lepidozamia peroffskyana employs a similar strategy. It is pollinated exclusively by host-specific Tranes weevils that spend their entire lives in the male cones, with occasional visits to female plants that result in fertilisation. Tranes weevils have also been identified as the pollinating insect for the eastern Australian cycad Macrozamia communis and the southern Queensland Macrozamia machinii. Specific thrip species (Cycadothrips) are involved with Macrozamia macdonnellii (Cycadothrips albrechti) of Central Australia and Macrozamia lucida (Cycadothrips chadwicki) of southern Queensland (Brisbane to Nambour) – while in the tropical north Bowenia spectabilis is associated with Miltotranes weevils. In many cases these pollinators appear to be species specific, suggesting an ancient association with their host plant (Terry 2005; Hall 2004; Mound & Terry 2001). Macrozamia communis (male cones).
Tranes lyterioides weevil and larvae. This insect is a specific pollinator for Macrozamia communis. (Images courtesy: Professor Rolf Oberprieler, CSIRO Ecosystem Sciences)
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Melanotranes internatus is a stem-boring weevil of Macrozamia and Lepidozamia. These weevils often use sick or damaged plants as breeding chambers – the larvae feed on the plant tissues and progressively ‘honeycomb’ the trunk, eventually killing the plant. (Image courtesy: Professor Rolf Oberprieler, CSIRO Ecosystem Sciences)
Melotranes weevils can become a pest because they are are highly resistant to presticides, breed prolifically and, due to their concealed lifestyle, are not easily identifiable in a plant. They will readily travel within wild plants (readily relocating with plant specimens shipped overseas) and can thereby contaminate urban gardens in transplanted Cycads. In a review of Lepidozamia peroffskyana Paul Kennedy comments: ‘Having seen evidence of Melotranes internatus on L. peroffskyana plants, it is my opinion that the purchase of L. peroffskyana plants taken from the wild (or the taking of any cycads from the wild) is somewhat like a lottery, with the chance that if you happen to end up with a plant that is infested with Melotranes internatus you may unknowingly have a mini-ecological “time bomb” on your hands’ (www.pacsoa.org. au/cycads/Lepidozamia/peroffskyana3.html). Yet another good reason for conserving wild plants in their bushland habitat.
A Rare Cycad-dependent Butterfly
Many butterflies dine on toxic plants – with the colours of the larvae and the butterflies acting as a warning (aposematism) that advertises their toxic defences. The Atala butterfly (Eumaeus atala), from the Caribbean
Atala butterfly, Eumaeus atala. (Courtesy: Scott Zona, flickr)
Eumaeus atala larva. (Courtesy: Patrick Coin)
and south Florida, selectively uses Zamia integrifolia as a host plant and source of defensive toxins.2 This butterfly was, until fairly recently, considered to be extinct. With urban development severely compromising its survival prospects, the butterfly re-established itself to some extent by using cultivated cycads as its food source. Even so, in Florida the Atala butterfly continues to be listed as endangered. The yellow-spotted orange-red larvae feed exclusively on the native Zamia cycad, which they can completely defoliate. This means they require large plant populations to survive. In the process the larvae store cycasin, which acts as a highly effective deterrent to predators at all stages of the butterfly’s development. Indeed, adults can store around 40 per cent cycasin in their wings, making them terribly distasteful. The yellow eggs and the orange-
2 There is some dispute over the classification of Zamia in Florida. Some classifications treat all the American populations as Zamia integrifolia, while others use Zamia pumila for the native Florida cycad.
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red pupae likewise contain considerable amounts of cycasin. Other butterfly species have a similar arrangement with Cycads, among them some Geometrid ‘looper’ moths from South Africa, which store cycasin and macrozamin from species of Encephalartos (Schneider 2002; Rothschild 1986). Indeed, recent studies have also shown that these azoxyglycoside toxins are also present in beetles feeding on the leaves of American species Zamia boliviana (Bolivia) and Dioon edule (Mexico) – an adaptation that appears to have been made long ago in the evolution of these ‘leaf beetles’ (Aulacoscelinae family) (Prado 2011). This suggests Australian insects would be no less adept at utilising cycad toxins for defence, which would doubtless be a fascinating subject for further investigation.
Zamia furfuracea and ripe seed cone. Zamia integrifolia showing seed cone.
Detailed studies of the American species Zamia integrifolia and Z. furfuracea showed that these cycads have selective weevil partners: Rhopalotria slossonae and R. mollis, respectively.3 The alluring scent of the male cones is specific:
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linalool and 1,3-octadiene in Z. furfuracea and methylsalicylate in Z. integrifolia – which appear to be activated by heat production by the cycad (Schneider 2002). 3 Pharaxonotha zamiae may be an additional species-specific pollinator of Z. integrifolia.
Persecution of an Ancient Plant
The evolutionary adjustments made by the Cycads over time have not been enough to ensure their future survival. Human influence on the process of environmental change has changed conditions across the continent. The clearing of vegetation for farming lands and sprawling urban developments have taken their toll on the limited habitats available for the native Cycads. Cycas media was once an abundant and common feature of the Australian landscape but over the decades wild populations have diminished significantly. As early as the 1880s, concerns regarding conservation issues were voiced by the botanist James Keyes: ‘This graceful and interesting species is gradually disappearing from the district, a circumstance which I attribute to the destruction of the cones by insects, of the young leaves by marsupials, and of whole plants, by boys, who often thoughtlessly cut them down or otherwise injure them when they came their way’ (Keyes 1886). Perhaps he should also have mentioned the wholesale clearing efforts of farmers, who were quite averse to having these plants on their land due to their known toxicity to stock. Until fairly recently, most Cycads were regarded as merely pestilential for this reason. Early incidents of Cycad poisoning in cattle were to provide a harsh learning experience for many farmers. Listed under Macrozamia spiralis, Burrawang seeds were found to be toxic to most farmed animals: ‘Cycads are particularly attractive to cattle during dry seasons because the leaves often remain fresh and green at these times. A similar situation exists in recently burnt country where new Macrozamia leaves might be almost the only food available. Field evidence indicates that young shoots are more toxic than older leaves. Dry leaves have been found to be much less toxic than green ones’ (Thieret 1958). Cycads’ toxicity was to lead to their destruction over
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Burrawang (Macrozamia spiralis) from the Botanical Magazine, 1872. This is a small species (60 cm high, 6–8 fronds) that is restricted to Richmond, north of Sydney. The closely related Macrozamia elegans, which was named in 1998 by Ken Hill, was formerly classified as M. spiralis. In much of the older literature Macrozamia spiralis probably refers to M. communis. This is because the species identification communis was not created until 1959, in a revision of Australian Zamiaceae by Dr LAS Johnson. Thus prior to this, various Cycads in New South Wales that were classified as M. spiralis subsequently fell under the M. communis umbrella – which differs because the latter is a large Cycad (up to 2 metres high) with numerous fronds (100 plus). Macrozamia montana and M. reducta were also formerly classified as M. communis. In addition, M. lucida in Queensland has often been misidentified as M. spiralis (further details available from www.pacsoa.org.au/cycads/ Macrozamia).
large areas of Australia that were utilised for grazing purposes. Massive tracts of land were repeatedly cleared of all Cycad species. Plants were usually grubbed out by the roots, although they could also be staked. The latter technique involved a sharp-pointed steel bar, or crow bar with a chisel end, which was used to split the stem. This allowed weathering and rotting of the plant, a strategy that was particularly effective during the rainy season. The use of kerosene or arsenic on the heart or crown was another method of killing ‘zamia palms’. Caulescent species (those with a well-developed aboveground stem) such as Macrozamia moorei were exposed to a different
Macrozamia communis (Burrawang) and Eucalyptus maculata (Spotted Gum) forest, near Bateman’s Bay, New South Wales. Burrawang can be found growing prolifically around this region, often in impressively dense stands – although numerous areas have now become cleared for urban development (Image courtesy: Russell Cumming)
eradication strategy, with a notch cut into the stem for administration of the poison (Thieret 1958). However, if plant debris was left lying around incidents of poisoning could still occur, and roots that were left in the ground could also regenerate. Even so, it was a difficult task to rid the countryside of these pestilential nuisances. In 1900 Joseph Maiden recounted an unusual case of stock poisoning that is illustrative of the problem. He drew attention to the effects on cattle of eating Macrozamia roots – a part of the plant to which the animals would not normally have access: A few weeks ago I was discussing ‘rickets’ in cattle with a prominent squatter who had an unfortunate experience with Macrozamias, for such is the botanical name for the blackfellows’ potatoes and burrawangs. They induce ‘rickets’ in stock, and the trying part of it is that stock get into the depraved habit of eating them, even if good feed be available. This squatter, during the winter of 1895, went to considerable expense in eradicating Macrozamias from a very large paddock. The plants, leaves, and roots were left lying on the ground. In 1896 stock were put back again into the paddock, and in six weeks stock (previously unaffected) were affected badly with ‘rickets’. Some of them were opened and their stomachs were found to be
CYCADS: PREHISTORIC SURVIVORS full of dried Macrozamia leaves. He closed the paddock to cattle for another twelve months, readmitted them and similar injurious effects occurred right up to April, 1898. During the three years the strewn-about leaves had finally disappeared, and cattle are eating the roots which are turnip-like in appearance, and which have been lying on the surface of the ground for the period stated. The effects of the roots on stock appear to be similar to those of leaves. The unfortunate stock-owner thought he had cleaned his paddock when he dug up all his Macrozamias by the roots. From which I have stated it is obvious that this is insufficient, as they must all be burnt – leaves roots and all. It seems sufficiently extraordinary that cattle should eat dried Macrozamia leaves, years old, exposed to all weathers; but it seems even more extraordinary to find stock eating the roots of this plant, a taste that can only have been acquired at a recent period, as Macrozamia roots are rarely removed and left lying in paddocks (Maiden 1900a).
This provided a serious warning against underestimating the toxicity of these plants.
Macrozamia moorei was said to ‘cause horses to stagger somewhat in their front legs, to step high, and, eventually, to become nearly blind’. This was initially attributed to seed toxicity, although it was later noted to be more in keeping with poisoning due to the leaf (Thieret 1958). (Image courtesy: KAW Williams, Native Plants of Queensland, Vol. 3)
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Macrozamia moorei, showing cut leaf bases at crown of cycad and epiphytic fern. (Courtesy: Wayne Atkinson)
Dioon: A Prehistoric Cycad Overseas, many Cycad communities have suffered disastrous losses from urban and farm development. Dioon is considered to belong to one of the more prehistoric classifications of the living Cycad genera. It is the most primitive member of the American Cycad complex, and Dioon fossils dated to around 36 million years have been found in Alaska. Although this habitat seems highly unlikely today, the find attests to the extent of climate change over the millennia. Dioon spinulosum is a tropical forest Cycad native to Mexico. Female plants produce an impressive silver-grey cone, among the largest of the Cycads, which becomes prostrate and hangs down after pollination. Although once widely established in the wild, the plant’s distribution has Female specimen of Dioon spinulosum. The Dioon genus, although not widely utilised, has had occasional cultural and dietary uses similar to the Australian Cycads. In Mexico young Dioon seeds were ground to a paste and used to make tortillas, while the old seeds provided toys. The leaves resembled palm fronds so closely that they regularly provided decorations for religious ceremonies such as the Palm Sunday celebrations.
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become highly restricted. Most of its natural range has been cleared and there are only a few survivors. Similar to the Australian Cycads, Dioon favour fire and have a rather remarkable capacity for regeneration. Hence, even after the land has been cleared and burnt a few individuals may manage to lead a hazardous and precarious existence on the fringes of farmlands. The odd Cycads seen on the edge of urban developments across the Australian continent have been similarly persecuted.
Ancient Survivors: Bowenia and Lepidozamia
Bowenia spectabilis, from the Botanical Magazine, 1872. The Australian genus Bowenia contains the smallest members of the Cycad family. The genus was named after the first Governor of Queensland, Sir George Ferguson Bowen, who was later to become Governor of Victoria.
Bowenia spectabilis is an elegant plant of the rainforest understorey that is found from Tully to Cooktown. It produces only two or three glossy leaves, with a fern-like appearance, that rise from the ground on long straight stems – from which it acquired the name Bowenia Fern or Zamia Fern.
The carrot-shaped tuber of Bowenia spectabilis ends to be well anchored into the soil, and it is difficult to remove entire. The tuber can also produce coralloid roots which, when cut, show dark masses of blue-green algae within.
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Bowenia is an extremely ancient genus, at least 45 million years old, which has endured almost unchanged over the millennia. These small fern-like plants are truly prehistoric, with a very different appearance to most other Cycads. Botanical evaluation has shown that the leaflets of the modern species differ little from those of fossil specimens of Bowenia eocenia and B. papillosa. There are two living species, Bowenia spectabilis and B. serrulata, which are restricted to central and northern Queensland.4 In contrast to their use of Cycas seeds, it was the rhizome of Bowenia that was eaten by Aboriginal people. It required detoxification and was crushed, washed and roasted before being made into a form of flour. The cones could be prepared similarly (Flecker 1948). The early settlers found that the Bowenia Cycads were stock poisons. The toxin of Bowenia spectabilis was noted to have a cumulative action resulting in irreversible weakness of the hindquarters in cattle – ‘Zamia staggers’ (Everist 1981). John Thieret (1958) noted: ‘Bowenia spectabilis is regarded as definitely poisonous to stock that graze upon the leaves … The poisonous nature of this species has been proved by feeding tests. Bowenia serrulata has been known to be very poisonous to cattle, resulting in lumbar paralysis. Macrozamin, the toxic crystalline substance first isolated from Macrozamia spiralis, has been found in Bowenia serrulata (what part not stated), while tests indicate that the seeds of B. spectabilis probably contain the principle.’ Zamia staggers was subsequently found to be widely associated with the toxic effects of various native Cycad species. Dr Thomas Lane Bancroft provided the following description: ‘The chief symptom of the disease is loss of proper control over the movements of the hind quarters. A rickety animal may run several yards without showing any peculiarity whatever, when suddenly it may drag its hind limbs, much like a dog sick from tick bite, or knuckle over upon its hind fetlocks, or may fall upon its haunches, immediately afterwards righting itself. Badly affected animals, when excited a good deal, may fall quite helpless for a minute or more, after which they get up and walk away as if nothing was amiss with them, and are even able to jump fences’ (Bancroft 1892, citing Anon.). 4 Bowenia sp. ‘Tinaroo’, found around Tinaroo Dam on the Atherton Tablelands (northern Queensland), was thought to potentially be a third species – however, it remains classified as Bowenia spectabilis.
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Toxin Strategies for Weevils ]
Fruiting specimen of Bowenia spectabilis.
Bowenia spectabilis: outside of female seed cone. (left) and mature seeds (right).
Immature female seed cone of Bowenia spectabilis showing internal structure.
Bowenia cones, which develop at ground level, have an intimate relationship with a
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specific weevil (a species of Miltotranes) to effect pollination. The seeds, which are quite large, have an ‘after-ripening’ period of 6–12 months. This means that although the seed is ripe, the embryo is immature and incapable of germination. It continues to develop during this period, and germination may not occur for 12–18 months. Recent studies have shown that the weevils that pollinate Bowenia have specific feeding habits that protect them from being poisoned by Cycad toxins. They do not feed on female cones – a few bite marks have been found on them, but the weevil does not appear to be partial to the taste and prefers male cones. The toxin in male cones is encapsulated in specialised cells within its tissues (in the female the deterrent toxin floods throughout the entire plant tissue) and the weevil is able to excrete the encapsulated toxin in its faeces. This means that safe food and brood sites are selectively available to the weevils in male cones. The female cones require the weevils to visit and deliver the male pollen, but they certainly do not require them to eat the next generation of Cycad seeds (Martin 1999).
The Byfield Fern (Bowenia serrulata) is found only in a few isolated coastal areas of central and northern Queensland, favouring the sandy and rocky soils of damp Eucalypt forests. This Cycad gained its name from a site at Byfield, north of Rockhampton, where
it is common. While the plant has a very similar appearance to the Bowenia Fern the leaves differ – the leaflets of the former having distinctive sharp-toothed edges (see page 360). The glossy leaves of the Byfield Fern grow from a large underground stem and sit atop slender stiff black stalks up to 60 cm tall. The Byfield Fern’s fronds vary in colour from yellowish green to a bright green, while those of the Bowenia Fern tend to be a consistently darker rainforest green.
Stangeria: A Magic, Ornamental and Medicinal Cycad The Stangeria genus has a unique botanical status, containing only one species, Stangeria eriopus (syn. S. paradoxa). It has a very interesting ancestry that is linked to the now extinct seed ferns, with ‘sun’ and ‘shade’ adapted leaves – a trait that is also reminiscent of some fossil ferns (Barbacka 1998). Indeed, similar to the Australian Bowenia, the plant was originally thought to be a fern and described as Lomaria in 1836, although this classification was revised in 1892. The species name eriopus refers to the velvety hairs that cover the young leaves. Stangeria’s ancestry can be traced to southern South America – with ancient plant fossils (Eostangeria pseudopteris) found in Wyoming and Oregon suggesting interesting links with prehistoric times. This complex area of study continues to have many intricacies that remain unresolved (Chaw 2005). Robert Buckley provides an insight into the significance of these plant lineages: ‘In Stangeria we have a cycadean relic of remarkable significance, a modern “missing link”. How fortunate for us that it has survived all those millions of years, along with the equally significant Chigua. In Eostangeria and its descendents we can see the dawn of not only Stangeria, Chigua, and Bowenia, but also Zamia and perhaps Microcycas, and Ceratozamia, as well. Thewitch doctors are right, Stangeria is indeed a magical cycad!’ (Buckley 1999).
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One Cycad of particular interest as a medicinal and magic plant is the South African Stangeria. The plant has had an extremely interesting magical reputation. The Zulu regarded it as having pretty strong protective actions and it was very valuable for ensuring property security. Powerfully repellent to evil spirits, the potion was said to erect an impenetrable barrier against those with sinister ambitions. Buried near the house, the root could even prevent lightning strikes.
Stangeria eriopus. From the Botanical Magazine, 1859.
There is an extremely interesting review by Roy Osborne and colleagues (1994) of the magical and medicinal usage of Stangeria eriopus in South
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Africa. Stangeria seed infusions have been utilised as an emetic to induce vomiting – a ‘cleansing’ action that rendered the person ‘invisible to harmful spirits’. On a more practical note, the Xhosa used its purging effects to induce vomiting in children who had accidentally taken poisons. Stangeria contains unusually high levels of sodium sulphate, which acts as an emetic. Another intriguing comment mentions the ‘nut’ being applied by natives to the integument of the penis ‘for a purpose on which the author does not speculate’ (Osborne 1994). Minor uses included its use a snuff to relieve congestion in infants, the burnt root powder for headache and as an ingredient in a decoction taken for an ‘illness beginning with a headache’. The tuber has also been utilised for ‘stomach winds, pain of the big bones, and aches and pains of the spinal cord’, which suggests that it may have an analgesic effect (Osborne 1994). The plant has also been utilised as a hypotensive agent and studies have shown ACE-inhibiting (angiotensinconverting enzyme) effects, which support this use of the plant (Duncan 1999). Unfortunately, Stangeria contains the toxic compounds cycasin and macrozamin. Although the toxin BMAA (β-N-methylamino-L-alanine) was not present, this suggests that infusions and other preparations could have considerable toxic potential. In addition, an interesting study has shown that the leaf flavones of Stangeria eriopus and a number of other cycads tend to be biflavones, similar to those found in Ginkgo biloba and some of the Araucariaceae – for example, amentoflavone, bilobetin, ginkgetin and isoginkgetin. Another flavone, hinokiflavone, is present in many of the Zamiaceae (Meurer-Grimes & Stevenson 1994; Dossaji 1973). This type of chemical investigation has interesting potential for tracing botanical links within different plant classifications. Stangeria eriopus has, like many species, been a casualty of clearing for farming operations, notably for pineapple and sugarcane crops. Illegal collection has compounded the threat to those that remain.
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The fern-like leaf structure of Stangeria is somewhat similar to the leaves of the Australian Bowenia, as are its growth habits – and both species placed in the ancient Stangeriaceae family. The leaf design of Stangeria differs, however, because it has a strong central midrib (that of Bowenia is much smaller) and the leaf, with its thin lateral veins, bears a resemblance to a bird’s feather. The following comment is of particular interest with regard to the ancestry of these Cycads: Actually, the leaves of Bowenia have taken the architecture of the big, fragile ferny Stangeria leaf a step farther by reducing the membrane of the major leaflets to a series of smaller leaflets extended out on subdivisions of a naked midrib. The result is a large photosynthetic surface area broken up into a number of small structural elements that are much less subject to damage from wind or rain. This technique of simulating a larger leaf surface by creating a spray of smaller leaflets is an advanced vegetative feature that apparently appeared in the Cretaceous since Bowenia fossils from the Eocene already show this leaf structure (Buckley 1999).
Male Lepidozamia Cycads produce bright orangered seeds that only the native rodents find edible in their natural state.5 However, the seeds have been used by Aboriginal people to make flour, utilising the same cautions and processing techniques that accompanied the use of other Cycads. There are only two species of this unique genus in Australia – the northern Queensland Lepidozamia hopei, and L. peroffskyana from northern New South Wales and southern Queensland. Two other Lepidozamia species are known only from fossil remains: L. hopeites and L. foveolata. Lepidozamia Cycads can be an impressive sight. One only has to appreciate the fact that they are very slow growing to be in awe of their great age.6 In 1873, at the entrance to the Mulgrave River near Cairns, George Dalrymple commented on an impressive specimen of this plant: ‘Catakidozamia Hopei [Lepidozamia hopei], W.H., upwards of sixty feet in height, with the trunk measuring seven feet in circumference three feet from the ground. This is the lowest situation in which I have found the latter
Hope’s Cycad (Lepidozamia hopei) has a limited distribution in the northern Queensland rainforests, being found only from Cardwell to the Bloomfield River. Some ancient individuals have been recorded growing to great height (13.7 m) and girth (2.36 m), with fronds up to 2.5 m long.
Stangeria leaves.
5 Carotenoids are probably responsible for much of the seed coat colour. Interestingly, the type of carotenoid present can differ, depending on the species: lycopene is present Zamia, and β-carotene in Encephalartos, Dioon and Macrozamia (Bauman & Yokohama 1976). 6 In general, the growth rate for Cycads is around a metre per 100 years (1 cm per year), although this can vary according to species, climatic and soil conditions.
CYCADS: PREHISTORIC SURVIVORS
Lepidozamia hopei was named after Captain Louis Hope, who was a major pioneer of the sugar industry in Queensland. Detail shows male cone scales.
Lepidozamia peroffskyana: showing new fronds and trunk detail. This Cycad was named in honour of Count Peroffsky by the Russian botanist Eduard August von Regel. An Imperial Russian minister might seem a rather odd choice of namesake for an Australian plant, but Count Peroffsky was a benefactor of the St Petersburg Botanic Garden where this species was first cultivated, and it was here that the original botanical description was made in 1857.
tree. The highest elevation in which I have seen it was four thousand feet above the sea. It is the grandest of the Cycadeae.’ It is likely that few, if any, of such impressive stature survive today.
The Genus Cycas
Cycas was the earliest Cycad genus scientifically described. It is thought to have originated in Laurasia
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and subsequently migrated throughout much of the Old World region. The genus ex-326 tends halfway around the globe and is found throughout Southeast Asia, India, the Malayan archipelago and the Pacific – ranging south to Australia and north to a few Japanese islands. The fact that Cycas are found in countries that span a massive distance Cycas media, fruiting plant. has presented serious obstacles to their study, some of which have been of a political nature. The extensive distribution of the genus has involved the evolution of species that favour selective habitats, with numerous unique species being found only in restricted, remote or inaccessible regions. Understandably, this has resulted in significant practical and logistical obstacles to their study. The issue has been further complicated by the fact that many Cycas species are extremely difficult to differentiate from each other and require expert identification. This can be a very complicated undertaking. Obtaining samples and transporting them to herbariums to permit detailed investigation can be a problematic exercise at the best of times. If the plant is rare, harvests can involve an added risk of site disruption or destruction, particularly with very small populations. There are a number of species that continue to be classified as ‘poorly understood’, and the very real threat of extinction looms over the existence of numerous others. In some countries botanical research has not been undertaken to any great extent, which means there are species that remain unclassified. In places like the Philippines, for example, which encompasses a massive area, so far only four species have been described. There are many unique habitats on these islands that suggest greater diversity is possible. Fortunately, in the last two decades major strides have been made to redress the problem. Estimates in the 1990s of the diversity of Cycas species placed the total number at around thirty. Today 95
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Cycas cairnsiana in the wild. (Courtesy: PI Forster, Queensland Herbarium) Cycas cairnsiana, a vulnerable species found only at a few sites around Mount Surprise, is one of the unusual ‘blue’ cycads. The plant was first collected in the 1870s, although it did not attract a lot of attention until the late 1980s, when it became extraordinarily popular with collectors.
The situation in Australia has been similar. Indeed, the tropical regions contain unique environments that have been an unexpected source of new species. In Queensland there are nine species of Cycas – of these six were first described by Ken Hill as recently as 1992. In 1995 Paul Forster of the Queensland Herbarium, Brisbane, wrote of the conservation concerns regarding these plants: ‘All but two of the Queensland species of Cycas are considered as rare or threatened plants … There continues to be indiscriminate poaching of populations of horticulturally desirable species such as C. megacarpa K.D.Hill, C. ophiolitica K.D.Hill, C. platyphylla K.D.Hill and C. cairnsiana F.Muell., while many populations of some species still suffer from uncontrolled land clearing for agriculture and grazing.’ Forster’s paper dealt with a previously unrecorded community of Cycas at Charters Towers that did not appear to fit the classification of Cycas cairnsiana. This was of considerable interest due to conservation concerns, and the plant was eventually classified as a new species, Cycas desolata (Forster 1995).
species are recognised.
Cycad Seed Harvests (Right and below) Cycas platyphylla, which has been known as the Petford Cycad, was once collected in extensive numbers as it was easily accessible to road traffic around Petford, near Mareeba, in northern Queensland. (Images courtesy: PI Forster, Queensland Herbarium)
Cycads once provided a seasonal food resource. However, they were not ‘cultivated’ in the normal manner, although sites were regularly visited and the crop harvested. There are some old sites in northern Queensland, around Cedar Bay and Jourama Falls, that can still be found today. Ludwig Leichhardt (1847) mentioned a Cycad grove on his travels in northern Australia: The scrub opened upon fine box flats, with numerous shallow watercourses; farther on … we met with some Cycas palms from thirty to fifty feet high, thick at the butt, and tapering gradually towards the crown. At one of the shallow creeks, which suddenly became rocky, and probably formed falls and rapids in the wet season, we struck upon a well beaten foot-path of the natives, which led us through Cypress pine thickets, and over open lawns to a creek, whose right bank was covered with Cycas groves of the most strikingly picturesque appearance; and here I observed that the Cycas, although it generally has a simple stem, frequently grew with two or three arms. The foot-path went up the creek … conducted us from one Zamia grove to another, which alternated with fine forest composed principally of white-gum, the fresh
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green foliage of which was extremely pleasing to the eye. I observed some large wells, ten or twelve feet deep, and eight or ten in diameter, which the natives had dug near the Zamia groves, but they were without the slightest indication of moisture.
A very old specimen of Cycas media, festooned with epiphytes, at the Flecker Botanic Gardens, Cairns. This cycad would probably be 200–300 years old. Willie Wagtail (Rhipidura leucophrys). Cycads could be a valuable ‘calendar plant’ for Aboriginal people. Indeed, when the tail feathers of the Willie Wagtail turned white the Cycad seeds were ripe. This signalled a time of the year when family groups returned to the coastal regions to begin their seasonal harvest (Tropical Topics 1994).
Fire Adaptation
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Fire stimulates Cycad seed crops and Aboriginal burning practices were deliberately intended to enhance crop production, with the seed yield from burnt Cycads estimated to be around seven times greater than that of unburnt plants. Fire-charred Cycad and Fire also helped to synchronise fruiting seeds. times and facilitated the harvest of old nuts which, after burning, could be readily located on the exposed ground. However, Aboriginal practices that intentionally favoured the fire-resistant Cycads could cause significant local environmental changes. In the rainforest, which is a fire-sensitive environment, vegetation changes could be particularly evident around cycad sites that had been deliberately burnt (Beaton 1982). Despite the fact that the native Cycads are adapted to living with fire, since European settlement fire has become a threat to many populations, particularly in the tropical woodlands. Fire frequency, which has increased as a result of some land management practices, can occur too frequently and the seeds are killed before they germinate. In many places this has resulted in serious disruption of the natural regeneration strategies of the forest (Hill 2003).
Burrawang
Burrawang is an Aboriginal name, from the Daruk language, that that has been applied to many of the Macrozamia genus – usually species that originate from New South Wales. On his Australasian travels in 1860 the naturalist George Bennett made the following interesting observations with regard to their use: The Microzamia [Macrozamia] forms a link between the Ferns and Palms, and is widely spread over Australia. The
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fronds of Microzamia, from their resemblance to Palms, are used in the Roman Catholic churches in New South Wales on Palm Sunday. The nuts of the Microzamia spiralis [Macrozamia spiralis, probably M. communis] are eaten by the blacks; they produce unpleasant effects, unless previously prepared by being steeped in water and roasted; but they form a poor article of diet, and are only used in seasons of scarcity. The stem underground is cylindrical and ovate, containing a quantity of a mucilaginous substance resembling gum tragacanth. This plant yields also a clear amber-coloured gum, and I have seen the fruit covered with it. The tuber of the Microzamia is of large size, covered externally with scales or leaf-scars, and, like the turnip, is a distension of the stem; the scales readily peel off: on the convex side, it is covered with a fine downy or silky substance; the concave side exhibits a shining orange-yellow colour, resembling very closely the scales on the trunk of the Xanthorrhoea; and on the upper part the remains of old fronds may be observed. The length of this tuber is 18 inches, with a circumference of 3 feet. The plants are dioecious, the male and female cones being on separate plants; they are generally found in rocky and sandy soils. It belongs to the family Cycadaceae.
The New South Wales Burrawang or Zamia Palm (Macrozamia spiralis) was one of the earliest Australian cycads to be classified botanically. It was originally described as a Zamia in 1796 and re-classified as Macrozamia in 1842. This specimen of Macrozamia spiralis is growing in the Botanischer Garten MünchenNymphenburg, Munich, Germany. (Image courtesy: Daderot, Wikipedia). There are over 40 species of Macrozamia in Australia, and the common name Burrawang has been applied to many of them. Macrozamia communis, the seeds of which are pictured here, is widespread along coastal New South Wales, ranging from Bega in the south, 600 kilometres north to Taree (although its distribution does not reach the northern coastline). (Image courtesy: AY Arktos, CC-by-SA 2.5, Wikimedia Commons project)
Cycads that resemble ferns
Zamia kickii from the Caribbean could easily be mistaken for a fern.
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Cycads that resemble small herbs or grasses
Zamia loddigesii (Mexico, Belize and Guatemala) could possibly be mistaken for a fern, although the leaf could also be considered palm-like.
Zamia pumila from the West Indies and Cuba.
The swamp fern Acrostichum speciosum has an almost Cycad-like appearance. Zamia paucijuga is a Mexican Cycad.
Zamia angustifolia from the Bahamas and Cuba.
Zamia vezquezii from Mexico.
Cycads that resemble palms
Zamia standleyi from Honduras.
Cycas media with epiphytes.
Fruiting Cycad showing a palm-like appearance
Zamia angustifolia from Icones plantarum rariorum, Vol. 3, 1786–1793, by Nikolaus Joseph Jacquin (www.botanicus.org/ page/271671). This species has the thinnest leaflets of the Zamia genus, and young plants can easily be mistaken for a grass.
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Starch from Cycads Many Cycads have a palm-like appearance and the term Cycas is allied to the Greek word for palm. However, the impression is mistaken as these families are completely unrelated. This has important toxicological implications. The nuts of many palms are edible, while those of the Cycad are definitely not. Indeed, the latter rank among the most highly toxic substances ever exploited as a food source. The only way Cycads could be successfully used in this way involved time-consuming and intricate processing methods. It is essential that the toxic compounds are completely removed. The techniques used to achieve this are considered to be among the most laborious and tedious processes that could possibly be employed – eventually yielding a white porridge-like starchy substance. In general this fare appears to have been regarded as a necessary source of sustenance rather than a culinary delight. It is important to realise that this meticulous processing is an essential prerequisite for the use of the seeds as a food. The consequences of inadequate processing can be both disabling and tragic – often causing the gradual development of painful, crippling and protracted debility. Eventually death results.
An Unanticipated Toxin
media. At the Endeavour River, Cooktown, he wrote: Palms here were of three different sorts … The third … was low, seldom ten feet in height, with small pennated leaves resembling those of some kinds of fern. Cabbage it had none but generally bore a plentifull Crop of nuts about the size of a large chestnut and rounder. By the hulls of these which we found plentifully near the Indian fires we were assured that these people eat them, and some of our gentlemen tried to do the same, but were deterred from a second experiment by a hearty fit of vomiting and purging which was the consequence of the first. The hogs however who were still shorter of provision than we were eat them heartily and we concluded their constitutions are stronger than ours …
Unfortunately this assumption was in error. He was later to note that the hogs: literally dyed after having eat them. It is probable however that these people have some method of Preparing them by which their poisonous quality is destroyed as the inhabitants of the East Indian Isles are said to do by boiling them and steeping them 24 hours in water, then drying them and using them to thicken broth; from whence it should seem that the poisonous quality lays intirely in the Juices, as it does in the roots of the Mandihocca or Cassada [Cassava] of the West Indies and that when thoroughly cleared of them the pulp remaining may be a wholesome and nutritious food.
This was a remarkably astute conclusion. Over the intervening centuries, subsequent episodes of animal poisoning implicating these plants have been reported in numerous journals.
Arrowroot from the Zamiaceae
Cycas media in fruit.
It is somewhat unexpected to find that the detoxification treatment of Cycad seeds was among the first observations made regarding Aboriginal life in Australia. As early as 1770, on Captain Cook’s original voyage, Joseph Banks commented on the use of Cycas
Zamia integrifolia.
The use of Cycad starch gained a measure of commercial success in Asia and the Americas. Joseph Maiden mentioned that in Florida the stems of a Cycad known as Koorti or Coontie (Zamia integrifolia7) were frequently ‘dug up for the purpose of obtaining the starch they contain, the finished product being an
7 Zamia pumila has also been known by the name Coontie.
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arrowroot of excellent quality’. In the 1950s a small starch extraction industry was established that produced and sold ‘Florida arrowroot’. Zamia integrifolia was once used throughout the West Indies by the nomadic Arawak Indians, who cultivated the plant during their journeys – which eventually led to its wider distribution. Unfortunately, today this Cycad has become increasingly rare in the wild. Major tracts of its habitat have been encroached upon by urban development. In addition, poaching from the wild (a harvest that tends to target large plants) has compounded the decimation of natural populations. Zamia integrifolia is now listed by CITES as being protected from international trade (Jones 1993). The procurement of starch was not only limited to Zamia integrifolia. In Australia Macrozamia riedlei also contains a substantial amount of starch in the stem, which the early settlers in Western Australia extracted by the following process: ‘The pith of the stem is dried either in the sun or by heating in an oven, shredded up and soaked in water for six hours. It is then shaken up Macrozamia riedlei, San Francisco Botanic and filtered, the milky fluid Gardens. (Image courtesy: being allowed to settle. The sediment is washed several Stan Shebs, Wikipedia) times, dried slowly, and finely powdered, and is ready for use’ (Carne 1926). The starch was not only utilised for food, it was also employed for laundry purposes, although it was not considered ‘sufficiently pure – it always contained a small amount of finely divided fibrous matter – to be an acceptable product on the market’ (Thieret 1958). The starch yield from the stem was 25–40 per cent in the moist plant and around 20 per cent fibrous material.
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Captain Cook and his colleagues were not the first
to suffer poisoning from the deceptive-appearing Cycad fruit. In 1646, some seventy years earlier, at the Swan River in Western Australia, Dutch explorers under the command of Willem De Vlamingh had sampled the delights of Macrozamia riedlei. One of the men recorded the following experience in the ship’s log: ‘I ate 5 or 6 of them … but after an interval of about 3 hours I and 5 others who had eaten of these fruits, began to vomit so violently that there was hardly any difference between us and death; so that it was with the greatest difficulty that I with the crew reached the shore’ (Robert 1972).
Macrozamia riedlei in the wild. (Courtesy: PI Forster, Queensland Herbarium)
Cycads continued to provide an unanticipated hazard for many Australian explorers. In 1839, George Grey and his party, who were shipwrecked at Gantheaume Bay on the Western Australian coast, faced a 480-kilometre trek to Perth.8 Rations were meagre and some members of his team made the same mistake as De Vlamingh’s men – eating Cycad nuts and suffering the inevitable, and unenviable, results. Fortunately they survived despite being ‘seized with violent fits of vomiting accompanied by vertigo and other distressing symptoms’. Although greatly weakened, ‘the poor fellows were still able to resume their march’ (Grey 1841). The whole venture sounded like a decidedly unpleasant undertaking. In 1892, members of an expedition led by Matthew Flinders suffered a similar experience at Lucky Bay in Western Australia. In 1847, in northern Queensland, Ludwig Leichhardt was equally unfortunate: ‘As we passed 8 Captain (later Sir) George Grey led two expeditions, both of which were plagued by disaster, that covered the Western Australian coastline.
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the Cycas groves, some of the dry fruit was found and tasted by several of my companions, upon whom it acted like a strong emetic, resembling in this particular the fruit of Zamia spiralis of New South Wales’. Cycad seeds and Pandanus were discovered at an Aboriginal camp. Leichhardt, like Joseph Banks before him, concluded that some form of preparation was necessary before they could be used as food. He keenly deduced the Aboriginal methods of detoxification: ‘I observed that seeds of Cycas were cut into very thin slices, about the size of a shilling, and these were spread out carefully on the ground to dry, after which, (as I saw in another camp a few days later) it seemed that the dry slices are put for several days in water, and, after a good soaking, are closely tied up in tea-tree bark to undergo a peculiar process of fermentation.’ At the next camp he found packets of soaked Cycas seeds that were undergoing fermentation: ‘They were of a mealy substance, and harmless; but had [a] musty taste and smell, resembling that of the common German cheese’.
Aboriginal Camp Resources
Ludwig Leichhardt was a keen observer of the environment through which he passed. He was particularly observant of conditions in the Aboriginal camps he visited and his descriptions often focused on their culinary resources. Cycad ‘nuts’ and Pandanus, as well as Emu meat, were among the foods found at one camp: After crossing the river … at last we came to a small tea-tree gully with two pools of water, near which some natives were encamped; there were, however, only two very old men in the camp at the time, who, on seeing us, began to chant their incantations. We were too anxious to examine the water to stand upon ceremony, and, when they saw us approach, they retired across the river to their friends, who were probably occupied at no great distance in collecting the seeds of Pandanus and Cycas. In the camp, we observed Cycad seeds sliced and drying on the ground; and some Pandanus seeds soaking in large vessels; emu bones were lying in the ashes, and the feet of the emu were rolled up and concealed between the tea-tree bark of the hut. A small packet contained red ochre to colour their bodies … There was also a very large stone tomahawk made of greenstone; and some fans of emu feathers.
Australian male Emu (not the female) is the parent that raises the Emu chicks. (Courtesy: djpmapleferryman, flickr, CC-by-2.0)
Dinewan the Emu, from Woggheeguy, Australian Aboriginal Legends, collected and written by K Langloh Parker.
The fact that Emu was on the menu is of interest as the fat contains fatty acids with substantial therapeutic benefits. While the Cycad and Pandanus seeds are a starchy component of the diet, Emu is a lean meat that would have provided essential protein elements. The high concentration of unsaturated fatty acids (70%) in Emu fat also has a significant oleic acid component (43–46%), with smaller amounts of other essential fatty acids: linoleic (10%), palmitic (23.5%) and linolenic (1%) (Lindsay 2010). The oil has shown cholesterol-lowering attributes (Wilson 2004) – as well as effective wound healing and anti-inflammatory properties that have provided a useful healing balm for campfire burns. Interestingly, studies have supported its efficacy, showing antiinflammatory effects and the promotion of skin regeneration. In addition, it has good anti-arthritic attributes, which can be enhanced in formulations by other components such as vitamin E (Qiu 2005; Li 2004; Yoganathan 2003; Lopez 1999; Whitehouse 1998; Snowden & Whitehouse 1997). Recent studies have also suggested that the anti-inflammatory effects of Emu oil could be of use, taken internally, for irritable bowel problems including gastroenteritis (viral, bacterial, parasitic), and
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mucositis (a condition that develops as a side-effect of chemotherapy) (Lindsay 2010; Howarth 2008).
Emu Oil. (Courtesy: Dreamtime Kullilla-Art)
Flour from African Encephalartos African Cycads, which have a similar toxic reputation to the native Australian plants, have also been prepared by a process of fermentation. RO Williams, in The Useful and Ornamental Plants Encephalartos transvenosus. of Zanzibar and Pemba (1949) described the use of Encephalartos hildebrandtii: ‘The spongy farinaceous centre of the trunk, gwede, is used in Zanzibar as food in times of shortage. It is prepared by chopping small pieces, then heaping for about a week, to allow fermentation to take place for the neutralization of certain toxic substances. They are then washed; preferably in hot water, and dried in the sun, after which they are pounded and used as porridge, or by putting the flour into boiling water and continuing the boiling for some time and then stirring into a thick paste known as ugali.’ Encephalartos transvenosus, pictured here, was likewise utilised as a famine food resource. Beer has even been prepared from the central portion of the stem (Thieret 1958). At Cape Hottentot (in the vicinity of Cape Town) the pith of Encephalartos longifolius was scooped out of the trunk, tied up in animal skins, and then buried for a few weeks to two months
African Encephalartos species have been utilised as a source of starch – although, fortunately, maize was to later replace this potentially deadly harvest as a staple dietary item.
to ferment. The doughy matter could then be used to bake a form of bread, which acquired the name Broodboom (Breadtree Cycad). The unwary, however, always ran the risk of poisoning. Deneys Reitz, in Commando, recounts the story of General JC Smuts’ flight from the British troops to the Zuuberg Mountains during the Boer War. When supplies ran low some men sampled the wild pineapple-like fruit of ‘Hottentot bread’ (Encephalartos longifolius, formerly thought to be E. altensteinii). Reitz observed: I was astonished to find more than half our men groaning and retching on the ground in agony, some apparently at their last gasp. General Smuts was worse than the rest, so, with half our number out of action, we were also leaderless, for he was lying comatose … We had no food and could not move without abandoning the sick, so our position was critical. Commandant van Deventer was too ill to take charge … The sick men were worse than ever. General Smuts was very bad indeed, and van Deventer, his second in command, not much better… From the groans and cries on all sides it was clear that the sufferers could not travel … However, as darkness slowly passed, one man after another recovered sufficiently to stagger to his feet, and towards dawn there were not more than twenty unable to stand. General Smuts was still prostrate … He gave orders that the men who could not help themselves were to be tied to their saddle and that the commando was to march deeper into the mountains (Reitz 1929).
Another salutory lesson in the risks of trying bush tucker without the appropriate knowledge of its use.
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Old Cycas media seeds.
There was a painstaking sorting process that accompanied the selection of old Cycad seeds in Aboriginal traditions, which has been shown to lessen their toxic content. Shelled seeds were checked before being deemed suitable for use – those that were very shrivelled, hard to crush, or had an unpleasant aroma, were discarded. Analysis of naturally aged seeds found they contained one-tenth the amount of toxin (cycasin) in comparison to fresh seeds. Those discarded in the sorting process were found to have a higher content of cycasin (0.95– 0.54 mg/100 g fresh weight). In comparison, the sorted edible seeds contained no cycasin. Deliberately aged seeds (dried, prolonged storage or buried in the ground for some months) also contained less cycasin than bush-collected specimens. This certainly points to the fact that Aboriginal people (particularly the women, who did most of the gathering) were adept at the detection and selection of low-toxin Cycad seeds (Beck 1992). However, later studies were to discover that other, less readily detectable poisons, were lurking within this starchy food resource. The methods utilised by Aboriginal people for processing Cycad fruits varied from place to place, with water availability having a major influence on the selection of processing technique. George Grey’s expedition journal provided some detailed information on the subject: The native women collect the nuts in the month of March, and having placed them in some shallow pool of water, they leave them to soak for several days. When they
have ascertained that the by-yu has been immersed in water for a sufficient time, they dig, in a dry, sandy place, holes which they call mar-dak. These holes are about the depth that a person’s arms can reach, and 1 foot in diameter; they line them with rushes and fill them up with the nuts, over which they sprinkle a little sand and then cover the holes nicely over with the tops of the grass trees. In about a fortnight the pulp which encases the nut becomes quite dry, and it is then fit to eat; but if eaten before that it produces the effects already described. The natives eat this pulp both raw and roasted; in the latter state it tastes quite as well as a chestnut. The process which these nuts undergo in the hands of the natives has no effect upon the kernel, which still acts both as an emetic and cathartic (quoted in Maiden 1900b).
Experimentally, the raw nuts had disastrous consequences: gastrointestinal and liver injury, central nervous system disorders and death. The extent of the poisoning and the after-effects depended on the amount of toxin present. As the early explorers had found, the instant purging effects of the nut was an obvious deterrent to human experimentation. Because the Cycad toxin was relatively quick-acting and its effects were highly demonstrable, any defects in foodprocessing techniques would be readily apparent. Even so, the more subtle effects of long-term poisoning from exposure to trace amounts of toxins would be much more difficult to determine. It took over a century before the toxic Cycad chemicals were isolated and named azoxyglycosides.
Traditions from Antiquity
The methods employed in the preparation of Cycad starch are rooted in antiquity. A great deal of experimentation would have preceded the safe use of cycads. The complex processing ultimately deployed would have been originally applied to plants that were not necessarily toxic, in an effort to make them palatable. The bitterness of root crops such as Yam (Dioscorea species) can be removed by washing, while starch could be extracted from the tubers of others, such as those of the Black Lily (Tacca leontopetaloides), which provided a form of arrowroot (see Chapter 2). These would have been invaluable lessons in the strategies involved in food preparation. Flavour was not the only desirable attribute – grain and texture contribute greatly to the acceptability of a food resource. It would be a logical step to find
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that experimentation with food processing would also reduce the toxicity of other plants – somehow leading to the discovery of methods that could reduce the unpleasant side-effects of Cycads. This was an important development that allowed accessibility to a previously unusable food resource – one that was to become of great value during times of scarcity. The choice between starvation or poisoning was thereby avoided. Indeed, Cycad processing methods are more than 4,000 years old. Australian archaeological sites tend to verify the culinary use of Cycads from at least 4,300 years ago. It is likely that knowledge regarding their use is older. Cycad husks dated around 13,000 years old have been found at other sites, although they were not processed by washing to leach out the toxins. The fermentation of old seeds (which are less toxic) was another strategy that could reduce toxin exposure. Nevertheless, whatever method was employed, processing was an essential prerequisite to their safe use. Cycas media was widely utilised in the Australian tropics. In 1889 Carl Lumholtz described its use in northern Queensland: In the evening when Willy and Chinaman came back from their wives, they brought a basket of fruit from the poisonous palm Cycas media, which is called by the natives
Cycad seeds contain oil, sometimes in considerable amounts, that has been compared to palm oil – e.g. 28.2 per cent of a bright orange oil was extracted from the fleshy layer of Macrozamia riedlei seeds. The oil from the seeds of Sotetsu (Cycas revoluta), which contained reasonably high levels (20.44–23.37%), was used on Okinawa during food shortages in World War II (Thieret 1958). However, the inherent toxicity of Cycad products would doubtless preclude the oil from general use as a food product. Little appears to be known regarding potential industrial applications. (Image courtesy: Jan Vytopil – Czech Cycads, www.cykasy.czwww. cykasy).
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kadjera. When the nut is cracked, the kernel is subjected to an elaborate process of pounding, roasting and soaking, until all is changed into a white porridge. Although my men were very fond of my fare, which I shared with them plentifully, still they felt a need of their own food. Kadjera constitutes during this season of the year, from October to December, the principal food of the blacks, tobola and koraddan, other fruits, being what they live chiefly upon from January to March. When the time comes for harvesting these fruits, the women set out together to gather and prepare them, and they are frequently absent from the camp for several days.
Cycas and Macrozamia were employed similarly throughout other parts of the country. Walter Roth provided meticulous details of the processing involved: On the Bloomfield River it [Cycas media] is fit to eat from July to January. The nuts are gathered by old men, women and girls. They are roasted and cracked, the kernels being kept for some four or five days before being pounded up into flour by the women. The reason for letting these few days elapse is said to lie in the fact that the delay helps to make them pound up more finely. The pounded nut is next sifted through a palm-fibre dilly-bag, which, having a mesh with smaller interspaces than the other varieties of bag, prevents the coarser particles getting through. The flour is next put into a grass dilly-bag, which has been previously folded inwards upon itself, so as to form a basin-like receptacle, and placed near a stream. With the help of leaves acting as a trough, water is allowed to continue flowing into the receptacle, matters being so regulated that the water never overflows the edges. Fresh water is thus continually percolating through the Zamia flour in its dilly-bag colander, right through the night, and in the morning it is ready to be eaten. It may, however, be kept for some three or four days, up to which time it is believed to improve; it will not, however, keep good any longer than that [R Hislop]. On the lower Tully River it is steamed and cut up like the Castanospermum australe, but rushing water is made to fall from a height on to the content of the dilly-bag held below, so as to keep the mass both strained and well stirred – a process which is kept up continually for quite a day (Roth 1901).
In 1883 Edward Palmer mentioned the use of the ‘Dwarf Zamia’ at the Mitchell River in northern Queensland: ‘Encephalartos miquelii: grows on stony ridges a few feet high, along the coast near Cooktown, and through the Wide Bay district. Bears a large cone fruit, not unlike a pineapple. The seeds, when ripe,
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Damper from Cycas armstrongii Cycas armstrongii.
Macrozamia miquelii, Mount Archer National Cycas media subsp. banksii, Park, Rockhampton. Cooktown, northern Queens- (Courtesy: Ethel Aardvark, land. Wikipedia)
are orange red; they are baked in the ashes first, and the kernels are soaked in the water for several days, and being pounded and roasted, experience tells them when they are fit for eating.’ Macrozamia miquelii, which is certainly found along the central–south Queensland coast, cannot be the species to which Palmer is referring in the northern tropics. There are a number of Cycas species found in the Cooktown area, although Cycas media is very prevalent.
This small Northern Territory Cycad yields ripe orange fruit. These were collected, sun-dried and chipped into small pieces, which were placed in a string bag and soaked in running water for five days. This was then pounded to a coarse paste or flour and was made into small rolls, wrapped in paperbark sheets and, finally, cooked on hot coals in an earth oven. The resultant damper, which had a strong odour and heavy character, was regarded as good provender for long journeys. The bread also had good keeping qualities and could be stored for several months before use (Yunupinu 1995). In some areas Cycad seeds were cooked before being water-soaked, while in other areas fresh seeds were left soaking in still water as a storage strategy. This allowed their use up to five months later. Leached nuts can lose quite a substantial amount of starch during the washing process (up to 50%), thereby reducing protein and energy values (Beck 1992).
Macrozamia: Arrowroot Extraction Joseph Maiden mentioned the use of Burrawang seeds from Macrozamia spiralis (formerly Zamia spiralis, Encephalartos spiralis) for starch extraction (although he is probably referring to the species now known as M. communis):
Macrozamia communis.
This species is found in enormous numbers in the poor sandstone country between Nelligen and Braidwood [New South Wales] and other places in the southern part of the Colony. The quantity of nuts produced by these plants is simply prodigious; they contain a useful starch, but this is rarely utilised. The starch is occasionally exhibited at various Agricultural shows. For instance, on one occasion at one show at Braidwood there was exhibited quite a large quantity of the farina, some 50 lb weight, which could not be distinguished by appearance from the arrowroot ordinarily sold in the shops … The exhibitor stated that
CYCADS: PREHISTORIC SURVIVORS his family were in the habit of using it daily, and had done so for years, and had found it very nutritious. He crushed the nuts in some homely fashion, and allowed the starch to settle in large tubs of pure water, after which it was spread out to dry (Maiden 1900b).
The following correspondence provided greater detail regarding the process of arrowroot extraction from this Cycad. In a letter to the editor of the New South Wales Medical Gazette (November 5, 1871) Henry Moss of Shoalhaven noted: I received a bronze medal and diploma from the Paris Exhibition, for sample of arrowroot manufactured from the Burrawang nut. It is my opinion that a similar oil (called poison) is found in the commercial arrowroot as exists in the Burrawang. The same means to free the one from this pernicious oil is exercised by running it off with fresh supplies of pure water. What I sent to Paris was manufactured very simply – I had the shells broken from the nuts, then placed in tubs of pure water and pounded quite soft with a wooden rammer; then roughly strained to get all the debris of the nut away; then strained through fine cheese cloth, and the liquid allowed to stand for 48 hours in a long cask, plenty of fresh water being added in the interval. I had spile holes made in the cask within a few inches of the bottom, so that the water could be drawn off without disturbing the sediment in any way. After draining and re-adding pure water several times, until the oil disappeared, then the arrowroot formed a cake at the bottom. The water was then all drawn off, the cake of arrowroot cut out and dried in the sun, and then, when dry, reduced fine by rolling. Nothing more was required. The arrowroot is equal to any commercial arrowroot. I sent a fine sample, about 4 or 6 lbs weight, to the Exhibition in Sydney last year … I think it would pay first rate for a company to go into the affair. From experiments lately made … I believe Burrawang contains a great percentage of arrowroot.
These early investigations inspired attempts at commercial exploitation of Cycad starch. A review of the natural products industry in the 1950s by Professor HH McKern noted: Starch has been manufactured in NSW from Macrozamia spiralis [probably M. communis], a cycad occurring in great abundance on the south coast of that state. It is a palm-like plant with a thick stem, which, like many other cycads in other countries, is rich in starch. The plentiful occurrence of this species, commonly known as the ‘Burrawang palm’, in the Bateman’s Bay district of NSW led in 1921 to the establishment of a company to manufacture starch from
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this plant. A factory was erected on the Clyde River some 12 or 13 miles upstream from Nelligen, and from the inner portion of the stem of the palm 28–30% of starch was obtained. The starch was manufactured by grinding the central portion of the stem with water; the liquid was then run over silk sieves which retained fibrous matter, but permitted the starch grains to pass. The starch was purified further by washing and it was then allowed to settle. This venture prospered for a while, but according to Penfold certain technical difficulties forced it to close. Efforts are made from time to time to re-commence operations, but so far with no success (McKern 1960).
For laundering purposes Burrawang starch was of interest because it was found to be 50–70 per cent stronger than corn or rice starch: ‘Rice starch consists of very fine grains, while corn starch is much coarser. [Macrozamia] starch grains are of various sizes from very fine (similar to rice) to coarser particles approaching the size of those of corn. The fact that the grains of burrawang starch are graded accounts for the strength of this starch. The fine grains penetrate into the body of the fabric while the coarser ones remain on the surface. The starch, then, gives strength just where it is needed in the fabric.’ The residual starch was used for conversion into a commercial adhesive paste. In 1934 the market was very good, with around 10 tons being manufactured and sold on a daily basis (Thieret 1958). However, its use for laundering lost favour due to a slight brown stain that developed in the starch particles after drying, a discolouration that could not be removed economically. It was not only these technical difficulties that led to the closure of the operation – labour costs became prohibitive and the enterprise lost its viability. John Thieret mentioned another commercial venture in which the stems could be used to produce alcohol. Burrawang therefore received consideration as a starch resource for conversion to power alcohol. There was, however, a problem due to a substantial variation in starch content from plant to plant, as well as from site to site. Starch levels ranged from as low as 13 per cent to 25–30 per cent: ‘such figures may also vary depending upon whether the outer or inner core of the stem or the whole stem is analyzed. A transfer of starchy material from the outer to the inner core apparently takes place at certain times of the year with the result that the inner core is the richer in starch at these periods.’ This variation meant that some resources
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were found to be quite unsuitable: ‘Stems from one area (Murwillumbah) were found to be useless as a source of alcohol because of their low starch content, while those from Bateman’s Bay had a much higher starch content and so were of considerably more value as an alcohol source.’ Overall, investigations of potential markets for the product concluded that the Burrawang was better left as a resource for use only in times of emergency. The high fibre content of the stem (especially the outer core) was a serious hindrance to starch extraction: ‘Until some use can be found for the fibre, or until it can be proved advantageous to hydrolyze it completely, attention must be confined to the inner core as a source of alcohol’. Ultimately the cost of the harvest of the stem exceeded the price manufacturers could afford, making the venture unprofitable (Thieret 1958). While Aboriginal people processed Cycad fruits for starch, little use seems to have been made of the trunk of the plant. Baron von Mueller commented: ‘Curiously enough the original occupants of the soil seemed never to have made use of the copious starch, which can be readily washed out of comminuted stems of any Cycadaceous plants’ (Maiden 1900b). In contrast, the Japanese Fern or Sago Palm (Cycas revoluta) was widely employed overseas as a source of starch during times of scarcity, such as World War II or following typhoons, when crops could be devastated. The fibrous trunk was cut up, soaked and then dried to extract the starch, which was ground into a fine powder. Fermentation, which was a well-known method used to reduce the toxicity, has been employed in Guam, Vietnam, India, Indonesia and East Africa.
The Sago Palm
Sago preparation involves debarking the wickedly spiked trunk, which is then cut into small pieces. These are sun-dried, fermented and then washed repeatedly – the material ‘placed in a bamboo basket and leached many times with water’. The water is then caught in a wooden tube and the starch allowed to settle out. The resultant product had a high starch (44.5%) and protein (9.15%) content. Male plants of Cycas revoluta were usually harvested because they had a higher starch content – although this could vary from 27 per cent in October to 61 per cent in June (average 50 per
In Japan the Japanese Fern or Sago Palm (Cycas revoluta) is a popular ornamental bonsai plant. Thisspecies was formerly very highly regarded as a sago food resource and in some places security guards were employed to stop poaching. So greatly valued were these plants that those caught smuggling incurred an instant death penalty. Cycas circinalis and C. rumphii were equally suitable for sago starch extraction.
cent). The female stem averaged only 26 per cent: ‘starch content of the stem is greatly affected by seed production, apparently more than a year being required to synthesize the amount of starch consumed therein’ (Thieret 1958). The yield of starch from a Cycas stem 1.2 m long is equivalent to the annual seed yield of a single female plant (2.26 kg of starch extracted from around 550 seeds). Most Cycas species can yield large amounts of starch at around seven years old. The best time for harvest involved the selection of trees before fruiting, just before the flush of new leaves. However, Thieret made the point that: ‘There would appear to be no good reason – other than custom – for the destruction of entire Cycas plants to obtain starch from their stems – an unfortunate way to exploit a food plant of such slow growth, especially since the extraction of starch from the seeds is said to be more economical.’
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A Hazardous Crop
Cycads have continued to be utilised on some southern Japanese islands (Amami, Okinawa) for the preparation of miso paste. In the past the safety of this product was not always assured. Incidents of poisoning have long been associated with its use, due to the seeds being inadequately washed, leaving residual toxins in the starch. In 1952, a report by DG Haring provided some enlightening details: [The] value [of cycads] to the Amamians … is as a backlog when other crops fail through drought or storm damage – occurrences all too frequent. So the large orange nuts that grow in a cluster atop the stems of cycads are harvested, shelled, dried, and ground to a sort of meal as a reserve against emergencies. Cycad meal is prepared variously, mixed with other foods to stretch them out, and made into sake – and universally disliked.9 In addition, as noted previously, it is slightly poisonous and every now and then a batch of especial potency kills those who eat or drink the product. In famine or near-famine, however, any food counts and aversions are discounted in favour of survival. In slavery days cycads had to enter more largely into the diet than now, since nearly all land was used to grow sugar for export. In connection with cycads, another menace looms large. The poisonous habu vipers often nest atop cycads and lay their eggs among the nuts. When a peasant reaches up to gather the nuts, the snake strikes, and one more death swells the total. This adds one more reason why the cycad is disliked even though it provides emergency food and liquor. It is apparent that the good housewife who listed her menus said nothing about the dishes containing cycad; she serves them only in extremis, although she probably keeps the meal on hand.
Indeed, Amamians even used the nickname ‘Cycad Hell’ for their island abode. In a comprehensive review of cycasin, Professor Iwano Hirono (1987) outlined further details of poisoning due to the Cycad paste in Japan: Toxicity to man has generally been attributed to improper washing of the cycad nuts or stem. Acute intoxication in humans caused by cycads has occasionally occurred accidentally in the Okinawa Islands. In most cases, intoxication occurred after eating cycad ojiya, a kind of gruel boiled with bean paste or soy sauce. The latent 9 Thieret commented: ‘The taste [of this sake] has been described as bitter like strychnine and quite long-lasting. Those who drink the sake sometimes become violently ill or even die; for this reason the brew is called doku sake – poison sake.’
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time from the ingestion of cycad ojiya to the appearance of symptoms was 12 to 24 [hours] in most cases … In humans, the first sign of intoxication was the sudden development of nausea and vomiting. The victims then rapidly became unconscious, and most of them died within 20 [hours] after the appearance of the first sign of intoxication. In most victims, swelling of the liver was observed, and one victim who regained consciousness developed jaundice.
The False Sago Palm (Cycas circinalis) is distributed from India, Burma, Thailand, Sri Lanka, Malaysia and Indonesia, extending to some South Pacific islands. This species was known to have toxic qualities and crushed seeds have been used as a fish poison in Cambodia. In Celebes (Sulawesi) the juice from Cycas seeds was given as a drink to unwanted children ‘to kill them. This was done in instances in which the parents whished to continue, unburdened by a family, their nomadic way of life in the forests’10 (Thieret 1958). (Image on left courtesy: L Shyamal, Wikimedia Commons, GFDL CC-by-SA 3.0) 10 The source of Thieret’s information was K Heyne, De nuttige planten van Nederlandsch Indie I, 2nd edition, Batavia, 1927.
Cycas rumphii
The original botanical collection of Cycas rumphii from the Moluccas occurred in 1859 – although the plant is very difficult to differentiate from C. circinalis, which had been collected the previous year from the Malabar coast of southwestern India. Cycas rumphii differs from C. circinalis
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botanical circles. These cycads are native to India, Sri Lanka, Malaysia, Indonesia, the Moluccas, as well as a number of Pacific islands (Guam, Fiji, New Caledonia, Solomon Islands) and Papua New Guinea – regions with a tropical climate similar to that of northern Queensland (Jones 1993).
The Medicinal Side of Cycads Cycas rumphii – female plant at the Berlin Botanical Garden. (Courtesy: Gunther Fuchs) Cycas rumphii (tree trunk). (Courtesy: Robert Stein III, CCby-SA 3.0)
in that it produces impressively large seeds and possesses a few slightly different botanical features (shorter leaves, fewer leaflets etc.). Both species yield buoyant seeds that are readily distributed by ocean currents, and are generally found growing along the coast. They have a comparable distribution and have been regarded as the same species in some
Cycas seemannii is a fairly widespread Cycad that favours a coastal habitat in the western Pacific: New Caledonia, Vanuatu, Fiji and Tonga. It is one of the species that was once classified as Cycas circinalis (subsp. seemannii) or Cycas rumphii (forma seemannii), and was also listed as Cycas neocaledonica. It is considered vulnerable as its habitat has been continually disturbed by agricultural ventures.
Aside from their culinary and toxic reputations, Cycads have been widely used for medicinal purposes – although, in the light of modern investigations of their toxicity, all such applications must now be regarded as highly hazardous. In general, the therapeutic use of these plants has lapsed into obscurity, with few records remaining of their past deployment. Among these records is a mention of an unusual remedy that was employed by Australian Aboriginals in Arnhem Land. T Theodor Webb (1933) recorded the following treatment of spear wounds: ‘for wounds such as those inflicted by iron- or stone-headed spears the male flower stalk of the woragar (cycad) is used. This is split open and the soft centre obtained, which is cut into small pieces placed in a dzakarun, paper-bark basket, mixed with urine, warmed by dropping a hot stone into it, and then applied to the wound.’ The usefulness of the remedy remains unknown – although investigations of the seeds of Cycad species such as Cycas circinalis and C. media have shown strong antibiotic activities. Whether the flower stalks have similar potential is a point of conjecture that could possibly have some bearing on the validity of the spear-wound treatment. Certainly, the part of the plant utilised does appear to influence its antibacterial potential. Dr Nancy Atkinson (1956) found that the outer nut shell of Cycas circinalis was positive against Salmonella typhi and Staphylococcus aureus. The nut kernel, however, was much more strongly active against these bacteria, as well as Mycobacterium phlei. No activity was found in the growing point, leaf bases, fronds or inner corky layer of the nut. Similarly, no activity was seen in the outer layer of the nut or the leaves of Cycas media, although the nut kernel and the nut shell were strongly active against all three bacteria. Lepidozamia hopei (listed as Macrozamia hopei) nut kernel likewise
CYCADS: PREHISTORIC SURVIVORS
had good antibacterial activity against Salmonella typhi and Staphylococcus aureus, but was not active against mycobacteria.
Cycad seeds are composed of an outer layer (the sarcotesta) which has a fleshy character. The adjacent hard shell layer is the sclerotesta – which encases a starchy kernel (the female gametophyte and the embryo). In Australia, the sarcotesta could sometimes be eaten without preparation by Aboriginal people, while the kernel was cooked before use (Beck 1992).
Macrozamia pauli-guilielmi, a small rare cycad from the southern coastal regions of Queensland, was one of the species associated with inducing ‘zamia staggers’ – and the leaves (under certain conditions) were noted to cause ‘considerable liver damage, with a severe terminal fibrosis of that organ’ (Thieret 1958). The nut kernel of has shown positive antibacterial activity against Salmonella typhi and Staphylococcus aureus (Atkinson 1956). Macrozamia pauliguiliemi has been known by local farmers as the ‘Twisted Rickets Weed’ due to the twisting habit of its leaves and its stock poison reputation. (Image courtesy PI Forster, Queensland Herbarium)
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The use of Cycad seeds for treating ulcerous conditions, sores, swellings, wounds, boils and diverse skin conditions was once a widespread practice throughout Southeast Asia and the South Pacific. • In Papua New Guinea the crushed seeds of Cycas circinalis and C. rumphii, which have a very similar distribution and appearance, were applied to tropical ulcers – a treatment that was said to be very effective (Holdsworth & Lacanienta 1981; Woodley 1991). • The False Sago Palm (Cycas circinalis) was likewise used in Burma, Singapore and Malaysia to treat sores and ulceration (Burkill 1935). • Cycas rumphii was used for treating tropical ulcers on Manus Island and in New Ireland – on the latter island the moist core of the fruit was ‘placed inside a cleaned tropical ulcer’ (Holdsworth 1983). Additionally, the scraped bark, mixed with coconut flesh, was eaten to soothe ulcers of the mouth, throat and stomach. • In Vietnam and nearby regions, the fresh grated seeds were applied to malignant ulcers (Sundarraro 1993). • In India the resin was utilised for the same purpose. The seed (but not the leaf ) of the False Sago Palm (Cycas circinalis) has shown moderate antibacterial activity (Sundarraro 1993). The Japanese Fern Palm (Cycas revoluta) has • demonstrated antifungal activity in experiments involving mould contamination of seeds (Kumar 1990). • In Malaysia, Cycas revoluta bark was poulticed on swellings (Quisumbing 1951). • In Cambodia the mucilaginous terminal bud of Cycas circinalis was crushed in rice water, or in water containing a suspension of fine clay particles, as a dressing for ulcerated wounds, swollen glands and boils (Thieret 1958). A number of Cycads have been of limited importance as folk remedies for other conditions: • In the Central Province of Papua New Guinea, Cycad leaves were boiled and the tea drunk to soothe cough (Holdsworth 1987). • The dried bracts (scales) of Cycas revoluta contained an ‘albuminous and mucilaginous matter soluble in water’. This can be used to produce a gum
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resembling tragacanth (a gummy substance used in pharmacy as a binding agent) (Quisumbing 1951). The male bracts of Cycas revoluta earned a reputation having narcotic, stimulant and ‘aphrodisiac’ properties (Quisumbing 1951). The abundant pollen of Cycas rumphii was noted to have strong narcotic properties (Ridley 1911) and the male cone scales (bracts) were sold in Indian bazaars as an anodyne (Drury 1873). In Indian traditional medicine the fruit-bearing female cone of Cycas revoluta was made into a poultice and applied locally to relieve kidney (nephritic) pain (Quisumbing 1951; Drury 1873). In the former Dutch East Indies (Indonesia) a juice from the mucilaginous young leaves of Cycas revoluta was used a remedy for treating flatulence and to stop vomiting blood (haematemesis) (Chopra 1956; Quisumbing 1951; Burkill 1931). Indonesia (Java): a decoction of young Cycas seeds provided an emetic and was said to have stomach purifying properties (Thieret 1958) Ceylon: Cycas seed flour (boiled and eaten) was highly esteemed as a remedy for bowel complains and haemorrhoids (Ondaatje 1862).
leading to a gum that had expanded 50–100 times its original size – taking on the appearance of a ‘quivering colourless jelly’ that was comparable to Acacia or cherry gums. Some of the Cycad gums were said to be edible, including various African Encephalartos species. Interestingly, Cycad gums also had adhesive attributes – as well as a good reputation as an antidote for snake and insect bites (Thieret 1958). Mucilage can have unique chemical and physical properties which are species specific. It is particularly interesting to find that monosaccharides (arabinosa, fucose, galactose, mannose, rhamnose, methylrhamnose) in the Cycad mucilage can be used to differentiate the evolutionary history of various genera and their family relationships (De Luca 1982).
Cycads in Chinese Medicine Traditions Japanese Fern Palm (Cycas revoluta)
Gum and Mucilage from Cycads
Gum exudations from Cycads have been of interest for their rather remarkable swelling capacity: ‘When placed in water Cycas gum begins to swell almost immediately. By the end of several days, it expands to many times its original size and becomes so colourless and transparent that it cannot be seen in water but must be felt for with a rod. Cycas gum has been likened in its properties to that of Sterculia tomentosa’. The gum has had a few medicinal uses – mainly as a drawing agent that was ‘said to produce rapid suppuration when applied to malignant ulcers’ (Thieret 1958). In 1843 James Backhouse observed exudations of gum from Macrozamia spiralis, and in 1855 macrozamia gum ‘as fine as amber’ was exhibited in Europe. This type of gum (gum tears or flattened scaly pieces) was noted to have similar properties to that of Cycas. Placed in water, it could continue to swell over several days,
Cycas revoluta seeds. (Courtesy: Tato Grasso, Palermo)
Chinese medicine employed the ‘down’ on the young leaves of the Japanese Fern Palm, as well as the woolly bracts (which bear female spores), as a styptic to stop bleeding wounds. The seeds have had diverse uses associated with tonic, expectorant (to expel phlegm), emmenagogic (to promote menstrual flow) and antirheumatic (to ease pain) activity. There was a popular belief that the starch from the stem and seeds had rejuvenating actions
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and promoted longevity. However, unprocessed, it retained the toxic properties common to all these plants. In the early 1990s an incident of accidental poisoning of three dogs was traced to eating the stem of this plant. After vomiting their signs were depressed and they experienced severe congestion of the mucous membranes, thirst, profuse salivation and blood cell abnormalities. Fortunately they recovered (Botha 1991). Traditional Chinese medicine probably has the most extensive records of the therapeutic use of Cycads, usually based on Cycas revoluta. Meticulous processing was employed to minimise toxic reactions. In Hong Kong the roots were regarded as having a stimulant effect on the circulation and provided an antirheumatic remedy. They were also recommended for the treatment of pulmonary tuberculosis with haemoptysis (spitting blood), toothache, lumbago, leucorrhoea and traumatic injuries. The flowers had analgesic actions and were employed for treating dysmenorrhoea (painful menstruation) and epigastric pain, as well as being regarded as a useful tonic for genitourinary tract problems. They were specifically employed to conserve ‘seminal fluid’ in men and were used to treat nocturnal ejaculation – while for women it provided a remedy for leucorrhoea (vaginal discharge). The leaves have been recommended as a haemostatic, anti-inflammatory and analgesic agent. They were utilised in a wide range of disorders including haemorrhage, gastritis (stomach inflammation), peptic ulcers, hypertension, neuralgia11 (nerve pain), and even cancer. The seeds have also been used for treating hypertension (Hong Kong CMRI 1984b). The fact that Cycad leaves gained a reputation in Chinese medical practice as a useful anticancer agent is of particular interest. Dai-zhao Zhang (1989) noted that its properties included ‘activating’ the blood, relieving swelling, transforming phlegm, and eliminating dampness. It was employed in cancer of the lung, stomach, liver, uterus, cervix and nasopharyngeal region. Minyi Chang (1992) lists the properties of the herb as ‘being sweet, slightly warm 11 A seed decoction of Dioon edule was also said to be employed in Mexico for the treatment of neuralgia (Martinez 1933).
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and a little poisonous … used to promote blood circulation, eliminate blood stasis, dispel the wind and remove toxic materials’. Historically, ‘the drug calms the liver and cures all kinds of pains caused by liver Qi [energy]’. The herb was listed for use in cancers of the breast, penis, stomach, liver, lip and skin. It was well known that Cycad seeds and the plant crown had poisonous properties and that special processing, or herbal combinations, was required to minimise toxic reactions. The herb was therefore generally employed in combination formulations, which allowed a greater degree of flexibility in the use of the medicine. Combinations of different herbs, some of which could modify the toxic activity of various constituents in the formulation, were employed. The percentage of the individual components used could therefore change according to the needs of the individual prescription. Some of these treatments have been subjected to serious investigation. Since 1960 Japanese researchers have been studying the anti-cancer effects of cycasin, although the inherent toxicity due to the high doses required has been a substantial obstacle to its practical use.12 Aromatase inhibitors are among the compounds that have shown potential in oestrogen-dependent tumours. One study showed that leaf extracts of five Cycads contained these enzyme inhibitors – Cycas cairnsiana, C. revoluta, C. rumphii, Dioon spinulosum13 and Encephalartos ferox (Kowalska 1995). Though it appears that, for the present, the therapeutic use of these plants is best avoided, it is possible that future research may reveal properties of Cycad chemicals that could have practical uses. For instance, a cancerous compound derived from cycasin (DMH-2HCl: 1,2-Dimethylhydrazine-HCl) has already been used to induce experimental cancers, notably colon cancer, for the study of cancer biochemistry and the effects of chemopreventive agents employed in cancer treatment 12 Instances of poisoning continue to be associated from individuals selfmedicating, probably due to inadequate preparation. Simply washing and cooking the seeds may not be enough to completely remove the toxins. Twenty-one cases of cycas seed poisoning were reported in Taiwan between 1990 and 2001. The majority of sufferers thought the seeds were edible and exploited them for culinary purposes – a few were using it as a cancer cure, as a tonic or gastrointestinal remedy, as well as for cosmetic purposes. The main symptoms were gastrointestinal distress characterised by severe vomiting. All recovered within 24 hours and were discharged from hospital (Chang 2005). 13 In particular, Dioon spinulosum contained fairly potent enzyme inhibitors.
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(Castleden & Shilkin 1979).This would not be the first time that poisonous plants have been responsible for some remarkable medical advances. Strange episodes of beneficial drug development have already proven to be an integral part of the history of medicine.
The Decorative Cycad Macrozamia fraseri is a found in a limited region of southern Western Australia (near Perth). Although rare in cultivation, it is a highly decorative native species that will develop a dense woolly crown. (Image courtesy: Drew Devereux)
Cycads can yield a fine fibre known as ‘palm wool’ from the top of the trunk and the leaf bases, mainly sourced from species of Macrozamia and Cycas. This has been used as a stuffing for pillows and mattresses. The bark could be employed for making cordage, twine and thatch – and the wood for toy making, whistles, plates and small turnery
Cycad growing in Cairo, Egypt.
items. The hollowed seeds were even made into snuffboxes and matchboxes. Cycad leaves have been useful for making cloth or for weaving items such as hats, baskets, mats, fences and broommaking. The leaves were also used for artistic purposes – dried, preserved and hand-painted. Post World War II, leaf harvesting became a fairly big export business for ornamental purposes – making decorations such as wreaths, flower arrangements, and the artificial palm trees in window displays. The dried leaves were packed in large bales: bales of small leaves (20–30 cm long) contained around 26,000 leaves, while those with large leaves (80–90 cm) packed 5,000. In the 1950s around 1000 bales were exported annually from Japan. The market was highly profitable – with more than 3 million Cycas leaves being imported to the United States, valued at $30,000. It is perhaps unexpected to find that many Cycad species even provided decorations for religious ceremonies, notably Palm Sunday celebrations in Australia, the Philippines and India (Goa). They were also utilised in funeral processions in Dresden, Germany (Thieret 1958).
• There are numerous ingenious uses of Cycads that attest to their cultural significance across the world. These include the production of wool, cloth, decorations, ornaments and their use in religious rites. While the poisonous consequences of Cycad utilisation were an all-too-obvious deterrent to their use, there was an assumption that the deployment of intricate and meticulous processing traditions resulted in a safe product. However, the risk of poisoning never quite abated. The next part of the tale of Cycad toxicology involves some of the most challenging chemical, toxicological and epidemiological investigations that have ever been undertaken. It is a story based on mystery, discovery, setbacks and a rather remarkable level of professional debate and continuing conflict. These investigations have resulted in some rather extraordinary, and totally unexpected, developments with profound implications for neurological disorders.
Chapter 11
NEUROTOXINS: PLANTS OF PERILOUS CONSEQUENCE Neurological disorders are extremely difficult to treat. This area of medicine has been long been associated with great mystery, which only began to be resolved when investigators started to unravel the biochemistry of the brain and the nervous system. Neurones were first described by the Czech anatomist and physiologist Jan Evangelista Purkyně in the 1830s; his discoveries were followed by the pioneering studies of Camillo Golgi and Santiago Ramón y Cajal in the 1900s involving neuronal pathways. It took the better part of the next century to unravel how electrical impulses worked. The development of the microscope was pivotal to many of these discoveries – as was the later development of technologies such as X-ray, electroencephalography (EEG) and CAT-scans.
Hieroglyph for ‘brain’ from the Edwin Smith Papyrus (17th century BC). (Wikipedia)
Egyptian mummy kept in the Vatican Museums. In Ancient Egypt, the brain was normally removed during the process of mummification as the heart was considered be the centre of intelligence. The Egyptians were superb anatomists, however, and the ancient surgical document known as the Edwin Smith Papyrus (written in the 17th century BC), which is the earliest record that mentions the brain, provides full details of two individuals with head wounds involving compound fractures of the skull. The papyrus ‘contains the first descriptions of the cranial sutures, the meninges, the external surface of the brain, the cerebrospinal fluid, and the intracranial pulsations. It also contains the first accounts of surgical stitching and of various types of dressings’ (Wilkins 1964). (Image courtesy: Joshua Sherurcij) 385
Practical information on neurological functioning has also resulted from the use of many plant substances. The discovery of the therapeutic value of analgesics (particularly those of an opioid nature), anaesthetics and sedatives is intimately linked to plant products. Indeed, the interaction between various natural toxins and neurological disorders has been characterised by some highly enigmatic and intricate puzzles. Certainly, the continuing story of the Cycad toxins presents a convoluted tale, providing a particularly intriguing and complex illustration of chemical intricacies and unwitting exposure that involves some unexpected links to the world around us. This has led to unforeseen toxicological discoveries, the full import of which remain unresolved. Toxins that are present in a number of the Legume family (Fabaceae or Leguminosae) resemble those found in Cycads and also have the potential to inflict serious neurological distress. The key to their inactivation, as with Cycads, lies in processing methods that minimise toxin exposure. There are a number of related issues of interest with regard to neurological disorders that also involve dietary exposure – this includes some remarkably virulent toxins from fish and cyanobacteria, acetogenins from Annonaceous fruits (including the Soursop), and cyanide exposure from
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Cassava and various stone fruits of the Prunus genus (Rosaceae family). These stories continue to suggest that the world around us has far greater chemical potential than we have hitherto appreciated – with an extraordinary impact on human affairs.
Cycads at Kakadu National Park, Northern Territory – ancient plants in an ancient land. (Courtesy: Carol Boland)
Cycad Toxins
It is not surprising to find that investigations over the last few decades have actively discouraged many of the folk uses of Cycads, a large proportion of which relied on detoxification procedures. Over time the risk arises of some techniques being forgotten or less rigorously applied and the relationship between the plant and the development of disease may become obscured. This could lead to a situation resulting in partial and progressive toxicity due to incomplete processing. Something as simple as inadequate washing of seeds or starch can leave residual toxins in the diet. Research has even traced toxic reactions to remedies that could be considered inconsequential, such as the external use of cycad leaf poultices. While the toxicity of Cycads and
Cycas revoluta and male cone.
their relationship to neuronal disease is undoubted, the mechanism by which this happens has been subjected to extensive debate. Even today, there are those who remain unsatisfied with the level of proof that has been proffered to the scientific community. The chemical investigation of the toxic principles of Cycads began well over a century ago, in the 1870s. These investigations were plagued by difficulty. Some fifty years later Professor EH Rennie enumerated some of the problems: Occasionally plants have been reported poisonous but on close examination no poison can be found. An interesting case in point is that of Macrozamia spiralis, an Australian cycad. Several other species of the genus are known and their fruits and roots, containing as they do, large quantities of starch, are used often as food by the aboriginals, but, it is said, only after treatment such as is used in the preparation of arrowroot from cassava viz., crushing and washing for some time in a stream of water, with subsequent drying and heating. Petrie made a most exhaustive examination of the leaves and fruits, but failed to find anything poisonous. American chemists also failed to find anything injurious in a Floridan [sic] species, though it was poisonous in an untreated condition. Various theories have been propounded to explain the facts, but all have proved unsatisfactory when tests supposed to be crucial have been applied. It is perhaps possible that there is some very unstable substance present which undergoes decomposition in the process used to detect it, but it is difficult to imagine what kind of material it can be (Rennie 1926).
In the early 1900s formaldehyde was detected in Cycas revoluta, and in 1941 the glycoside macrozamin was isolated from Macrozamia spiralis by JM Cooper. More than a decade later, in 1955, the toxic compound cycasin was identified in Cycas revoluta by the Japanese scientist Kotaro Nishida and his research team. It was present in all the above-ground parts of the Cycad – and was identified in Cycas circinalis a year later by Riggs (Spatz 1969). This was to prove to be merely the beginning of a very tricky chemical puzzle. The true extent of the poisonous potential of these plants was not to become fully apparent to the world until medical attention was directed toward the high incidence of a debilitating disease on the island of Guam. Investigation implicated the False Sago Palm (Cycas circinalis, later classified as C. micronesica), which was extensively used as a source of starch.
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Intricacies of a Poisonous Puzzle
Macrozamia spiralis; illustration by Adam Forster, 1921. The New South Wales Burrawang or Zamia Palm (Macrozamia spiralis) was one of the earliest Australian cycads to be classified botanically. It was originally described as a Zamia in 1796 and re-classified as Macrozamia in 1842. The name spiralis refers to the spiral characteristic of the leaf stalk (the rachis).
Three female Cycas circinalis at Charles University Botanical Garden in Prague. The large specimen is 200 years old. Female megasporophylls are visible on the smaller specimens. (Courtesy: PeregrinusX, CC-bySA 3.0, Wikimedia Commons project)
The presence among the Chamorro people of the island of Guam of the world’s highest incidence of the degenerative neurological condition (amyotrophic lateral sclerosis, ALS), and a Parkinsonism-dementia complex (PDC), was for long an unexplained mystery. The symptoms of this complex (today referred to by the acronym ALS-PDC), were extremely distressing and highly debilitating. Victims initially experienced a loss of muscular tone of the face, then progressive loss of function of the arms and legs. The severity of the muscular dystrophy progressed to the extreme where they became ‘living vegetables’, with death often occurring within five years. In some cases the paralysis and dementia was accompanied by the development of diabetes. Awareness of the toxic potential of Cycads led to suspicions among mid-twentieth century researchers regarding the dietary aetiology of the disorder. A pivotal observation for these researchers was the fact that Japanese soldiers stationed at Guam during World War II had also contracted the condition. Pioneering investigations in the early 1960s managed to associate the disease with the excessive consumption of Cycas starch (Whiting 1963). Indeed, the incidence of ALS among the Chamorro and other people using Cycad-derived starch in their diet was found to be almost a hundred times greater than the normal occurrence of the disorder.1 This vital discovery instigated the study of Cycad toxicity on an international scale. 1 Similar forms of ALS-PDC were reported from Irian Jaya (western New Guinea) in 1982, and from the Kii Peninsula (where it was known as Muro disease) of Honshu Island, Japan, in 1972 (Spencer 1987a, 1987b).
The Guam Neurological Disorder
Parkinson’s disease is a degenerative neurological disorder characterised by movement dysfunction: tremors when resting, rigidity, bradykinesia (slowed movements) and gait disturbance. Emotional dysfunction (mood changes, depression, apathy, anxiety) and dementia are not uncommon. The condition has a characteristic pattern of damage that involves dopaminergic pathways in the brain. However, the condition found on Guam (ALS-PDC) has a different presentation, and is composed of two separate
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disorders (Shaw & Hoglinger 2008; Shaw 2006): • Amyotrophic lateral sclerosis (ALS): is characterised by loss of voluntary movement, progressive muscle weakness, twitching and atrophy occur due to nerve cell degeneration in the central nervous system. • Atypical Parkinsonism dementia (PDC) – i.e. it was not the regular form that was associated with Parkinson’s disease. There is also an uncommon form of pigmentary retinopathy that occurs in individuals suffering PDC. The suggestion has been made that this may result from an interaction between BMAA (β-Nmethylamino-L-alanine) and melanin (Karlsson 2009). A small percentage of individuals were unfortunate enough to suffer from a combination of both conditions. It has been established that familial susceptibility plays a role in the development of ALS-PDC – although both disorders could be present in the same family (Shaw & Hoglinger 2008; Shaw 2006). While the incidence of ALS has markedly declined on Guam since the connection with Cycads was established, the prevalence of dementia among the elderly is still quite high. Clinically this form of dementia is equivalent to Alzheimer’s disease, albeit with some different pathological features (Galasko 2007). MRI scans are often normal in patients with ALS, although they can be a useful diagnostic tool to rule out other complicating conditions such as spinal cord tumour or herniated neck discs. While this MRI is hard for the novice to interpret, an expert would be able to discern changes in the motor cortex that are suggestive of ALS. (Image courtesy: Dr Frank Gaillard, Radiopaedia.org)
The results of early experiments involving Cycad toxins were extraordinarily difficult to interpret. They showed that the toxins caused the development of liver, kidney and intestinal cancers in animals – but there was no sign of nervous system dysfunction. Field observations, however, continued to point to Cycads being at the root of the problem. In addition, neurological problems such as paralysis of the hind legs and ataxia (incoordination of the gait) had been reported in animals, mainly cattle, grazing on land where Cycads were found. The species found on Guam, Cycas circinalis, was found to contain the carcinogen cycasin, which had previously been isolated from Cycas revoluta, the Japanese Fern Palm. While cycasin appeared to be implicated, the mechanism of action remained unknown, and the compounds responsible for the neurological complications remained a mystery. Experiments during the 1980s and early 1990s determined that the cycasin content of Cycads was highly variable: • 0.016% in washed, ground and dried nuts; • 2.3% in unwashed and vacuum dried nuts, which could be as high as 3.6% in different batches; the differences in some studies were dramatic: • cycasin concentrations could vary from 0.004– 75.93 mcg/g. e toxin BMAA (β-N-methylamino-L-alanine) was Th also isolated: • concentrations ranging from 0.00–18.39 mcg/g; • on the average, cycasin levels were around 10 times higher than the levels of BMAA. The finding that cycasin was readily soluble in water meant that starch or seeds which had been thoroughly soaked and washed could not be the source of the problem – at least as far as their content of this carcinogen was concerned. Properly prepared Cycad bean paste and starch contained no cycasin. Experiments confirmed these findings – rats maintained on a diet containing up to 10 per cent commercial cycad flour did not develop cancer. BMAA was likewise considered to be removed during processing (Kisby 1992; Spencer 1991a, 1991b; Duncan 1990; Hirono 1987; Hoffmann & Morgan 1984). Unravelling the pharmacology of cycasin was
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to prove to be a highly complicated challenge that, over many decades, was to involve the expertise of researchers from around the world. The cancerous potential of this compound was not understood until biochemists demonstrated that cycasin could be converted to a more toxic carcinogenic compound, MAM (methylazoxymethanol), by the intestinal flora. This was a vitally important finding that, for the first time, showed intestinal bacteria were a contributing factor in cancer development. The implications were profound for toxicological studies. Importantly, it meant that cycasin was active when administered orally, but not as an injection – thus researchers using the latter method of administration could not demonstrate the compound’s toxicity. The revelation that MAM appeared to be toxic regardless of the route of exposure highlighted the incredible disastrous potential of the metabolised compound. MAM also damaged pancreatic islet cells, which suggested its role as a ‘slow toxin’ in the development of diabetes mellitus (Spencer 2010; Eizirik 1996; Choi 1996; Eizirik & Kisby 1995; Hirono 1987; Campbell 1966). The situation is complex. While no doubt existed with regard to the toxicity of MAM and cycasin, and recent studies have supported their neurotoxic potential (Kisby 2011), several other glycosides have been identified with the potential to influence Cycas biochemistry. Even today, this continues to be the subject of extensive investigation. BMAA has neurotoxic properties, although the fact that its activity was not shown to be significant in a number of studies has confused the issue. Another rare amino acid, MeDAP (L-α-amino-β-methylaminopropionic acid), which is closely related to another Cycad toxin, NMDA (N-methyl-D-aspartate), was isolated as well. These compounds were also implicated in Cycad poisoning, as both caused experimental damage to the brain and spine resembling that seen on Guam (Spencer 1991a, 1991b; Kisby 1992, 1988; Duncan 1989; Emsley 1989; Perry 1989; Hoffmann & Morgan 1984). The neurotoxins responsible continue to be the subject of intense debate. The interaction between nutrients and toxins is another factor with unknown potential that could contribute to the complexity of the Cycad toxin puzzle. There have been a number of suggestions: • MeDAP may bind to copper and zinc, compounds
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An Alternative Toxin?
There is a suggestion that BMAA may not be the only active neurotoxin in cycad seeds (Snyder & Marler 2011). Steryl glycosides, which are lipid soluble, have shown neurotoxic properties resembling the syndrome found on Guam – and a compound called BSSG (β-sitosterol β-D glucoside) has been proposed as the culprit. The levels can range from 20–1,340 mcg/g. Not only is this compound highly neurotoxic, it has been responsible for delayed neurological damage in animal studies (Marler & Shaw 2010; Shaw & Hoglinger 2008; Tabata 2008; Borenstein 2007; Marler 2005). A similar effect has been shown for BMAA – which can also potentiate the neurological insult inflicted by other toxins. It may therefore turn out to be a matter of a synergistic toxicology with numerous parameters involved (Caller 2009; Cox 2009; Lobner 2007). that are normally present in the central nervous system in a very stable form in combination with glutamic acid. It has been proposed that, over many years, deactivation of these essential minerals could contribute to the development of permanent neurological damage. Glutamate levels were shown to increase after treatment with MAM, which could promote neuronal degeneration2 (Esclaire 1999; Emsley 1989). The neurotoxic properties of BMAA and steryl glycosides can likewise be mediated via glutamate metabolism (Papapetropoulos 2007). • Other nutritional influences of interest include toxic metals or mineral deficits. Bicarbonate levels may be an important consideration. The presence or absence of toxic co-factors (e.g. aluminium, manganese) or protective nutrients (e.g. calcium, magnesium) continues to be investigated (Durlach 1997). • While magnesium deficiency does not directly cause neurodegenerative disease, when combined with aluminium excess and calcium deficiency (which can occur in soil and water samples) it can contribute to the development of neurological damage (Durlach 1997). 2 Glutamate receptors resembling those found in the human brain are present in some plant species. This suggests a broader role for BMAA, which is structurally similar to glutamate, as a signalling protein in plants (Baluska 2010; Davenport 2002).
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• P rocessing methods can make further detrimental contributions to the situation. Zinc can be leached from the galvanised containers utilised in preparing Cycad flour samples. The resultant flours were shown to contain zinc levels that were considered toxic (Duncan 1992). This finding has implications for commercial flour processing. • Additionally, there are dietary factors that may require consideration. Nigerian investigations demonstrated that when cycasin was combined with a high-protein, high-fat diet there could be associated changes in colonic function that were not seen with a high-carbohydrate high-fibre diet. The latter diet appeared to have a protective action and lowered cholesterol levels (Eriyamremu 1995).
A Matter of Exposure
Cycas micronesica, female plant with developing seeds. (Courtesy: Thomas Marler)
Cycas micronesica. (Courtesy: Wayne Atkinson, flickr)
The Mariana Flying Fox (Pteropus mariannus) was once a regular part of the diet of the Chamorro people. The finding that these animals dined on the sarcotesta (the outside covering) of Cycad seeds did not seem
particularly important until studies investigating the presence of BMAA in Cycad seeds (Cycas micronesica) found very high levels. The BMAA level in the sarcotesta was 9 mcg/g which, although not huge, is still fairly high. But the level in the outer seed layer just within this covering was extraordinarily high (1,161 mcg/g). A few years ago alarm bells truly began to ring when the BMAA level in museum specimens of the animals was found to be almost three times this level (3,555 mcg/g)3 – which was comparable to the BMAA content of over 1 kilogram of processed Cycad flour. Incidentally, despite being processed, the residual level of toxin in the flour could vary substantially, depending on the efficacy of the washing technique used (Banack & Cox 2003; Cox 2005, 2003). It has since been established that even low concentrations of BMAA can cause the death of motor neurons in the nervous system, and it is possible that this level of exposure may act as a trigger for neurological disorders in genetically vulnerable individuals (Shen 2010; Pablo 2009; Steele & McGeer 2008; Banack 2007). At one stage, some aspects of the investigation into the cause of ALS-PDC stalled because of uncertainty regarding how washed Cycad flour (fadang) used for making tortillas in Guam could contribute a significant level of the toxin. The belief that the flour posed an insignificant exposure risk changed with the finding that acid hydrolysis allowed a considerable amount of BMAA to be released (169 mcg/g), whereas the measurement of free BMAA was negligible. When the BMAA was found to be bound to the protein fraction of the Cycad flour it was realised that the digestive process, or other metabolic functions, could facilitate its release – particularly upon exposure to the acid hydrolysis that normally occurs in the stomach. Later studies of protein-bound BMAA in washed Cycad flour gave levels that ranged from 24–33 mcg/g and 40–169 mcg/g – indicating the possibility of a fairly high level of exposure (7–30 times that 3 Museum specimens were selected for two reasons: they were collected when the ALS-PDC syndrome was prevalent five decades ago, and since 1973 the animals could no longer be legally hunted on Guam. Nonetheless, some Chamorro still regard Flying Fox as part of their traditional diet, albeit a hazardous choice. This line of enquiry regarding the significance of contaminated Flying Fox meat in the diet was not popular in various neurological circles and met with a great deal of disbelief. It continues to be regarded as contentious by some (see Marler & Shaw 2010; Steele & McGeer 2008; Borenstein 2007; Marler 2005).
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previously estimated4). In addition, flesh from other contaminated foragers could be included in the diet: pigs dine on Cycad seeds and tree stems, feral deer prefer the leaves and young sporophylls, terrestrial crabs eat toppled Cycad stems, and freshwater shrimp consume the outer integument of fallen seeds (Banack 2011, 2006; Marler & Shaw 2010; Shen 2010; Cheng & Banack 2009; Cox 2005, 2003; Murch 2004). The age of the seeds used for flour preparation has been another matter of interest. Young Cycas micronesica seeds have a higher concentration of toxins, notably steryl glycosides, in comparison to the mature, dark brown, older seeds. This factor probably relates to seed maturation, which is a long-term process taking around 20–24 months. It is notable that steryl glucosides levels in seeds that are no longer attached to the plant (harvested seeds or seeds lying on the ground) remain stable. Other toxic components in Cycads can have a similar variability. In Cycas micronesica cones the BMAA concentration was greater in the tissue of immature male cones, compared to mature cones (Marler & Shaw 2009a, 2009b). 4 It is important to appreciate that BMAA was extremely difficult to isolate. Increased levels of sophistication in analytical procedures needed to be developed before studies could confirm or deny the presence of BMAA in food, animal and human tissue. Recently a paper has been published on the use of triple quadrupole mass spectrometry (MS-MS) as a more sensitive and accurate procedure, with a 10-fold increase in sensitivity over older GCMS (gas chromatography mass spectrometry) methods (Esterhuizen-Londt 2011).
A Complex Species Identification
Cycas circinalis, showing male cones. (Image on left courtesy: Raul654 CC-by-SA 3.0, Wikimedia Commons project; image on right courtesy: Michal Mañas)
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Cycad seeds are fitted with a flotation layer that enables them to travel long distances on the ocean currents. The seeds can thus maintain their viability and tissue integrity, withstanding the rigours of being immersed in sea water for long periods – a strategy that has resulted in the widespread distribution of a number of species along the shores of India, Asia, Melanesia, and the Pacific Islands. Their diversity and inaccessibility meant that some ‘species complexes’ took a long time to classify botanically, which resulted in a lot of confusion in species classification. Cycas rumphii was originally thought to be more widespread than was eventually determined. Cycas circinalis has a similar distribution and was easily confused with C. rumphii, which is now considered to be restricted to a band of islands around the Moluccas – while C. circinalis is found only in India. Cycas micronesica, which belongs to the C. rumphii complex, is endemic to Guam and the surrounding islands (Marler 2005). In urban Guam, imported Cycas revoluta plants largely replaced the native species, although C. micronesica has recently become more popular. In 2003 both species were devastated by an imported scale insect (Aulacaspis yasumatsui). This led to the native species rating serious conservation concern and it was placed on the IUCN Red List in 2006 (Marler & Shaw 2009b). Cycas rumphii (male cone) at Berlin Botanical Garden. (Courtesy: Günter Fuchs CC-by-SA 3.0, Wikimedia Commons project)
Cycas rumphii (female).
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Cycas rumphii, illustrating female sporophylls and leaf.
Mariana Fruit Bat, Pteropus mariannus. (Image on left courtesy: Ann Hudgins, U.S. Fish and Wildlife Service; image on right courtesy: Christopher Todd, CNMI Division of Fish and Wildlife)
Some investigators proposed that the exclusion of Flying Foxes from the diet (which occurred when they were virtually hunted to extinction) was associated with the gradual decline in the incidence of neurological disorders on Guam (Cox & Sacks 2002). Others disagree, linking the condition to the ingestion of Cycad flour as young adults. During World War II, when many men fled the urban areas for the forest to avoid conscription by the Japanese, their preparation of this traditional food could easily have been less than meticulous in comparison to the way it was done in the home, thereby accounting for a higher occurrence of the disease in males (Marler & Shaw 2010; Borenstein 2007). Whatever the reason, the incidence of ALSPDC peaked as a major cause of death in the region in the 1940s. By 1960 it had become relatively rare, with only older adults found as sufferers. This tended to confirm an environmental or dietary link. Nevertheless, even today the presence of an increased incidence of dementia in Guam, and related cases of ALS-PDC elsewhere, suggests that the situation is by no means resolved. Cycad flour may not be the only risk factor involved (Steele & McGeer 2008).
presumably, have a high exposure to the toxin.5 The desirability of Flying Fox meat led to a massive decline in populations on Guam, where there were once two native species, Pteropus mariannus and P. tokudae. These animals were major pollinators and seed dispersers across the island. Over time Mariana Fruit Bat numbers decreased to the stage where the animal was listed as critically endangered. In 1968 Pteropus tokudae was consigned to extinction, with the killing of the last sighted female by hunters. In the 1970s, Pteropus mariannus was placed under ‘protective custody’ and hunting was subsequently banned on the island. By this time the fruit bat population had been reduced to around 100 individuals. Pteropus mariannus continues to be listed as a threatened species (www.fws.gov/pacificislands/ fauna/mariana-bat.html). With the dramatic loss of native Guam Flying Foxes, entrepreneurial types in Samoa and the Caroline Islands saw a market opening and began slaughtering their own wild populations for export to Guam. The trade involved some 20,000–29,000 carcasses annually, with cargoes peaking in the late 1970s. It has been estimated that 230,000 flying foxes belonging to 10 different species were imported to Guam between 1975 and 1990 (Cox & Sacks 2002; Chen 2002). Obviously, an unsuitable harvest. In Australia, Flying Foxes have been similarly
Guam Flying Foxes
The Flying Foxes do not eat the outer layer of the Cycad fruit – they squeeze the fluid from the sarcotesta and spit out the pulp. They can ingest considerable amounts of the juice and,
5 Marler (1995) disagrees with the toxic Flying Fox theory. He discusses their food preferences, seed chemistry, Cycad biology (including the role of symbiont fungi) and environmental factors for cycad growth in some detail.
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The Spectacled Flying Fox (Pteropus conspicillatus), which is native to Australia, New Guinea and some offshore islands, is very similar in appearance and size to the Mariana Fruit Bat.
persecuted, albeit for a different reason. Their foraging habits are not popular with fruit farmers and it is only recently that their slaughter has been banned. They too have an important environmental role as major pollinators of our forests, in particular the hardwood timber trees. Unfortunately, as urban settlements encroach on their traditional camping grounds they continue to be an unappreciated aspect of the natural environment. Certainly, the hazards of Cycad toxicity can be linked to the external medicinal use of Cycad seeds: The mature orange seed of the cycad tree, an indigenous plant scantily distributed in the forest surrounding the villages, was accepted by Auyu [Ainu] villagers [of Japan] as an ideal medicine for topical treatment (in individuals of all ages) of various skin lesions, including cuts, warts, abrasions, and open sores. For this purpose, scrapings of the starchy toxic inner portion of a raw seed are crushed by hand, the resulting pulp is immersed in the poisonous milky exudate, and the sodden mass is applied directly to the lesion on a leaf, which is then strapped in position. The poultice is replaced daily with freshly prepared pulp until the skin is healed. On a single occasion at the age of 15, one 29-year-old male with ALS (amyotrophic lateral sclerosis) of recent onset, was reported to apply the preparation to a 5–10 diameter open sore on the ankle for a month. An older brother with no clinical disease said he had used a cycad poultice for only 2 weeks to promote healing of a deep cut on one foot. Their mother, who had taught them the procedure, was ‘paralysed’ before death at age 50 and, according to the ALS patient, had the same disease (Spencer 1987a).
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It was extremely worrying that none of the people with neurological symptoms who were interviewed for the above report had taken the plant internally.6 The implications of these findings led to active discouragement of the use of Cycad-based medicinals throughout the entire region. There is also a possibility that chronic exposure from regular contact with Cycads in workplace situations such as plant nurseries or botanic gardens may result in a low level of poisoning. This could lead to a predisposition to certain disorders, or the gradual development of significant debility. This proposition has raised valid concerns, and recommendations to limit contact with these plants must be taken seriously. In a paper on the neurotoxic properties of Cycads the following advice was given: The presence of chemicals with toxic potential in practically all parts of cycads dictates the need for careful handling of these plants. Botanists working with cycads should recognise the hazard and minimise exposure. Chemical gloves should be worn when handling plant components and care should be taken to avoid dermal contact with seed juice and gum. Gloves also provide mechanical protection when handling cycad leaves. A tight fitting mask should be used to avoid inhalation exposure … clothing should be replaced at the earliest opportunity and exposed skin washed with soap and water. These simple precautions should minimise exposure to cycad chemicals (Spencer 1993).
The level of toxic components in these plants varies from species to species, and high levels would substantially influence the exposure risk. The mature leaves of a number of species contain azoxyglycosides (cycasin, macrozamin), while other species do not. There are studies that suggest a lot more research needs to be done to correctly evaluate the risk of toxin exposure in individual cycad species. One investigation of 32 species found quite variable results (Yagi 2004): • 18 species did not contain azoxyglycosides: Ceratozamia (2 of 3 species), Cycas (1 of 3 species), Dioon (3 species), Encephalartos (10 of 11 species), Macrozamia (1 of 3 species), Zamia (1 of 3 species). • 14 species tested positive, including: Bowenia (2), Ceratozamia (1), Cycas (2), Encephalartos (1), 6 Other researchers have not found any link between the use of the poultice and the onset of dementia (Borenstein 2007). Personally, I would not even consider exposing myself to the risk.
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Lepidozamia (2), Macrozamia (2), Microcycas (1), Stangeria (1) and Zamia (2). • The highest level of cycasin was found in Bowenia serrulata (2.16%), followed by Macrozamia miquelii (1.33%) and Zamia integrifolia (1%). • Cycasin levels were extremely low (range: 0.0011– 0.090%) in: Cycas circinalis, Encephalartos arenarius, E. trispinosus, E. villosus and Zamia fischeri. The level of macrozamin was also very low (range: 0.011– 0.38%). Species differences in toxic potential have also been demonstrated. Measurements of hydrolytic activity were used to indicate the potential of the plant material to release toxins from damaged leaf tissue7: • Mature leaves with a higher macrozamin hydrolytic activity: Dioon edule, Encephalartos villosus, Macrozamia miquellii and Zamia fischeri. • Leaf extracts oriented toward cycasin hydrolysis: Bowenia spectabilis, Stangeria eriops, Ceratozamia mexicana and Cycas revoluta. • Lepidozamia hopei: both toxins had fairly equal hydrolytic activity. • Just to confuse the issue, there were some conflicting results – Macrozamia miquellii leaf extract had a low hydrolytic activity toward cycasin, yet only cycasin was found in the leaves of this species. • Cycasin concentrations in the young leaves of Zamia and Encephalartos hopei were found to be higher than the older leaves (Rothschild 1986, Yagi 2004). • In addition, cycasin and macrozamin increased in Cycas revoluta leaf in the short term (1–2 months) – then declined in older leaves, with macrozamin becoming virtually undetectable. Both compounds were also found to be more abundant in the seeds of Encephalartos villosus, when compared to the leaf tissue (Yagi 1983 & 2004). • A comparison of BMAA in five different Cycads (species of Bowenia, Cycas and Dioon) found that the leaves of all five had greater tissue concentrations than did seed tissue (fresh weight) (Charlton 1992). 7 This is similar to measuring the cyanogenetic activity of cyanidecontaining plants, which is released as fumes upon tissue damage. It should be noted that Cycads also contain cyanide and can be classified as cyanogenic. However, no reports of human cyanide poisoning from Cycads have been documented (Chang 2005).
• Th e situation with Cycas micronesica appears to be the reverse, with seed tissue BMAA levels greatly exceeding that of the leaf tissue (Banack & Cox 2003).
Accidental Exposure
The toxic potential of the Cycad should not be underrated. Merely handling Cycad seeds (or the leaves) can result in serious poisoning. In the past the seeds have occasionally been given to children as toys or ornaments (e.g. marbles or necklaces), a practice with extremely hazardous potential. In children even a limited amount of exposure can have catastrophic conCycad seeds (Cycas media). sequences. The case of a young Japanese girl who had played with such ‘toys’ since birth provides a tragic illustration of the risk: ‘She developed into a healthy teenager and did well in long distance running races until, at the age of 18, she began to complain of backache and spasm of the calf muscles. At age 20, she was said to have leg weakness and her skin to have become translucent, and ALS was diagnosed [she died aged 25]. The disease appears to be less common in Iseji today, and children no longer play with sotetsu seed’ (Spencer 1987b).
A Cyanobacterial Link
There is a later chapter to the story of BMAA as a neurotoxin that came as something of a surprise to the entire scientific community. It began with the discovery that there was another avenue of BMAA production in the environment – via symbiont cyanobacteria (formerly known as blue-green algae) that were found living in Cycad roots.8 There is an element of biomagnification in the relationship
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because free-living cyanobacteria have much lower levels of this toxin (0.3 mcg/g) when compared to the level found in the coralloid roots (2–37 mcg/g) (Cox 2003). This discovery was to change the way the world viewed the impact of cyanobacteria on human health. Investigations that analysed the brain tissue of nine deceased Canadian Alzheimer’s patients found, surprisingly, that BMAA was present. For comparison, fourteen Canadians without neurodegenerative disease were examined at the same time and no BMAA was found. Follow-up showed that BMAA was present in the brain tissue of similar neurodegenerative cases from North America (University of Miami NPF Brain Endowment Bank, Florida). Thus a direct link between BMAA and neurological disorders began to appear. The fact that Cycad exposure was not a consideration suddenly implied that there was another environmental source of the neurotoxin. Cyanobacteria were the immediate suspects9 (Pablo 2009; Cox 2005). 8 Cyanobacteria have photosynthetic characteristics resembling algae, and can produce blue-pigmented proteins (phycobiliproteins). Hence their early description as blue-green algae, although genetically they are classified as true bacteria. They also contain gas vesicles, which give them buoyancy and light access in watery environments. 9 However, confusing the issue further, Cycas micronesica plants without cyanobacteria were also found to produce BMAA (Marler 2010).
Symbiotic Relationships
Cycas circinalis, showing coralloid roots. (Courtesy: peregrinusX, CC-by-SA 3.0, Wikimedia Commons project)
Cycads have a specially developed root system, with an unusual coral-like (coralloid) appearance, that has a very interesting relationship with cyanobacteria. In 1872
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J Reinke demonstrated the presence of an alga (Anabaena) in Cycad root nodules. Later studies expanded an understanding of the arrangement in Cycas revoluta: ‘The presence of bacteria in the nodules was demonstrated by Schneider [1894] Cycad roots. (Courtesy: Masahiko who considered Taniguchi, flickr) the alga, bacteria, and cycad to exist in a symbiotic relationship’ (Thieret 1958). The nitrogen-fixing relationship between cyanobacteria (Anabaena) and Cycas revoluta was discovered in the early 1920s, and French studies in the 1950s established that ‘cycad nodules with Anabaena contain more nitrogen than normal roots and that the alga is able to fix atmospheric nitrogen’ (Thieret 1958). This is of interest because Cycad roots attracted particular attention when it was found that BMAA (originally discovered in Cycas micronesica seeds) could be produced by the resident symbiotic cyanobacteria (Nostoc spp.) (Cox 2003). This association appears to be an important survival strategy, as it allowed Cycads to colonise habitats characterised by poor soil. It is probably an ancient evolutionary arrangement that allowed terrestrial plants to evolve independent of a watery habitat. Cycads have another odd habit. Their roots and stems can contract, which can pull the plant stem underground – an intriguing trick that some species can use to change their height by around 30 per cent (Martin 1999).
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Symbiotic relationships with cyanobacteria, which have long been known to exist in lichens and some ferns, have since been found in other plant species, along with the potential for BMAA formation. This has been of particular interest in Gunnera, the only genus in the family Gunneraceae and one of the very few flowering plants (Angiosperms) that have formed this association. In this case Nostoc punctiforme is the specific nitrogen-fixing symbiont, which infects the plant through specially formed stem glands. The strategy allows Gunnera to prosper in nitrogen-deficient soils, while the bacterium reaps the benefit of being able to source carbon from the plant (Chiu 2005; Bergman 1992). In particular, Gunnera kauaiensis and the water fern Azolla filiculoides contain BMAA derived from their cyanobacteria–plant symbionts (Cox 2005).
Pacific Mosquito Fern (Azolla filiculoides). Azolla symbionts are housed within specialised cavities within the fern leaves. The cyanobacteria include Cylindrospermopsis raciborskii, Anabaena cylindrica and A. oscillarioides (Papaerthimiou 2008). (Image courtesy: J Layton, CC-by-SA 3.0)
Gunnera kauaiensis. (Courtesy: Karl Magnacca, flickr)
Gunnera petaloidea is a large native Hawaiian rainforest plant that, like many in this genus, grows to impressive proportions: the leaves can reach 1.2 metres across, perched on stems 0.5–0.6 metres long. A single plant can spread over a large area (1.5–1.9 m2) and reach a height of 2 metres. (Image courtesy: Karl Magnacca, flickr)
However, the specific links between the dietary
use of various cyanobacteria, the production of BMAA, and resultant increased incidence of Parkinsonism-dementia remain unresolved. Nostoc is one example of an edible cyanobacterium that certainly enters into some traditional diets as its gelatin-like globules are easily harvested from local ponds. Nostoc flagelliforme soup is regularly eaten in Chengdu, China. Nostoc commune has been similarly used in Indonesian and Chinese traditions, as well as being fried as part of meat dishes, particularly with duck. In the Peruvian Highlands Nostoc commune can form a regular part of the diet, incorporated into stews, soups, salads or used as a snack food. Medicinally, it was macerated in water and taken as a remedy for fevers, ‘internal heat’, inflammation or applied locally for various pains (kidney, stomach, liver) and difficult childbirth. Its use, however, does not appear to be linked to a higher incidence of neurological disorders (Johnson 2008). Chinese concerns about exposure to BMAA has led to a ban on products made from Nostoc, although their traditional value as luxury foods has seen a lot of resistance to the idea (Roney 2009; Banack 2007). The result of regular exposure to BMAA from these sources in the diet, however, continues to remain an intricate and unresolved chemical puzzle.
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Pollen Exposure
Free-living colonies of Nostoc in a fresh-water pond in southern Oregon. Each colony forms a small sphere (about 0.5–1.0 cm in diameter). The tadpole is Pseudacris regilla, the Pacific Chorus Frog. The micrograph shows Nostoc filaments with specialised nitrogen-fixing cells known as heterocysts. (Images courtesy: David Dalton, Reed College, Oregon)
The problem illustrated by increasing levels of BMAA moving up the food chain – such as that occurring with the Flying Foxes of Guam – is called biomagnification. At least in some instances this was thought to have potential for significant increases in exposure. Part of the puzzle with regard to the development of dementia and paralysis on Guam appears to be linked to a ‘slow release’ of the toxin. BMAA can bind to proteins in the body that are gradually released over time during metabolic processes. In particular, protein-bound BMAA in the brain may act as a reservoir from which toxin release occurs, causing gradual neuronal cell death. BMAA has been found in the brain tissue of individuals who have died from ALS-PDC in Guam, which lends support to the theory that it is implicated in the
The Cycads of Guam produce prolific amounts of pollen that contains the toxins cycasin and BMAA.10 It has been postulated that there may be an olfactory route of exposure that could involve nasal damage from toxin inhalation. A combination of epithelial tissue damage, toxin exposure and metabolic change could permit toxins to reach the brain – which has the potential to result in neuronal damage (Seawright 1995). An appreciation of the massive problems that result from allergic rhinitis due to plant pollens would support the validity of this route of exposure – as well as the resultant severe systemic distress and immune dysfunction. The cumulative potential of contact with high levels of cycad pollen is thus worthy of consideration. While this area of investigation remains largely untouched, it is known that some cyanobacterial toxins can cause disease via inhalation. Brevitoxin, a neurotoxin from the fragile dinoflagellate Karenia brevis, can be aerosolised by the action of breaking waves on the beach. High levels of exposure are possible during episodes of ‘Florida Red Tide’ – blooms which have become recognised as a major health problem around the Gulf of Mexico (Fleming 2005).
Red tide off the Scripps Institution of Oceanography Pier, La Jolla, California. Courtesy: P Alejandro Díaz)
disease (Banack 2006; Cox 2005; Murch 2004). There is, however, still some debate about the exact mechanisms involved, how the damage occurs, and who is susceptible to the condition (Borensen 2007; Papapetropoulos 2007). 10 Interestingly, BSSG (β-sitosterol β-D glucoside) was not found in Cycad pollen (Marler & Shaw 2010).
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The BMAA–cyanobacteria link raises concerns regarding the impact that marine cyanobacteria can have on health, suggesting an extremely disturbing scenario. Changing environmental conditions due to human activity have already been linked to an increased occurrence of algal blooms. The problem of the Murray-Darling river complex is illustrative. In November 1991 this system saw the largest toxic river algal bloom in recorded Australian history – with a massive 1000-kilometre stretch of the Barwon and Darling rivers in New South Wales affected: ‘from the air it looked like a long ribbon of pea soup’.11 Over 1,600 cattle and sheep died and the bill for emergency water supplies to affected station properties and townships topped $1 million. This is only a small indication of the possible side-effects that can accompany environmental mismanagement. An increased incidence of algal bloom outbreaks has already been encountered globally – a sure warning that we cannot be complacent about the future integrity of the world’s rivers and oceans. The fact that cyanobacteria in algal blooms produce a range of cyanotoxins has long been linked to incidents of poisoning – an important issue with regard to fish stocks and water supplies. While, in the past, poisoning has been more likely to occur on a localised basis, notably from fish and shellfish neurotoxins, in the last few decades there have been incidents with more widespread exposure that warn of the increasing significance of the problem. In 1979 contaminated water supplies were responsible for the hospitalisation of almost 150 individuals (mainly children) in Australia.12 In Brazil, 76 kidney dialysis patients died from toxin exposure due to contaminated water in 1996. There is also a risk of toxic cyanobacterial contamination of spirulina food supplements.13 Indeed, some studies have reported microcystin contamination of spirulina at levels that 11 See Toxic Algal Blooms: a sign of rivers under stress (www.science.org/nova). 12 While this was widely publicised as being due to the presence of Cylindrospermopsis raciborskii in the Solomon Dam at Palm Island, Queensland, the culprit may also have been copper. Copper sulfate was used as a water treatment when the water level in the dam was low, which could have resulted in over-treatment. The fact that the contractor dumped the entire load of copper sulfate right next to the town water-supply pipe, rather than spreading it across the dam, would not have helped matters much (see Prociv 2004 for further details). 13 Spirulina is a nutritional supplement suitable for human and animal use that is made primarily from two non-toxic species of cyanobacteria: Arthrospira platensis and A. maxima.
merit concern (Dittmann & Wiegand 2006). Equally worrying are recent findings that suggest algal blooms can have endocrine disrupting effects, which could have serious ramifications for hormonal production and functioning (ACS 2011).
Cyanobacteria: A Riverine Hazard
Digitally colourised scanning electron micrograph (SEM) of an untreated water specimen showing various unidentified organisms that include bacteria, protozoa and algae. (Courtesy: CDC, Janice Haney Carr)
Cyanobacteria are truly ancient organisms. They are widespread across the planet, with fossils attesting to a history of at least 2500 million years. It was cyanobacteria that began the extraction of hydrogen from water, releasing oxygen as a by-product and produc-ing Earth’s atmosphere. Understandably, they are extremely hardy – and they have the ability to survive in just about any environment. Australia has the dubious claim to fame as the source of the first scientific report on a riverine cyanobacterial toxin bloom in 1878. The Adelaide assayer and chemist George Francis observed a thick scummy green growth (Nodularia spumigena) on Lake Alexandrina, a fresh-water lake at the mouth of the Murray River, that rendered the water ‘unwholesome’. Animals such as sheep, horses, dogs and pigs that drank the odious mix suffered a rapid, sometimes horrible, death (Stewart 2008). Cyanobacteria thrive under conditions that provide phosphorus and nitrogen – nutrients that enter the water supply in fairly large amounts from today’s lifestyle: waste from factories, sewage, and the run-off from
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farms, urban parks and lawns. This process is known as eutrophication. Household detergents are an excellent source of phosphorus and nitrogen. Algal blooms favour still-water sites such as dams, ponds and reservoirs, and slow-flowing rivers. Clogged and damaged riverine ecosystems, often with fish pests such as the European carp, are a recipe for future disasters. Various different cyanobacteria can be involved in algal blooms. In Australia three main classifications have been identified: Anabaena, Microcystis and Cylindrosperm-opsis. Anabaena circ-inalis is among the cyanobacteria found in the Murray-Darling Basin. Anabaena algae have a tightly curled appearance, Microcystis forms a spongelike blob, while Cylindrospermopsis takes the form of a straight filament of Water weeds in a ditch in cells and does not Cairns. form algal ‘scums’ like the others. Cylindrospermopsis can be located in a band several metres under the surface and therefore, while the contaminant may not be visible, it can still be lurking in the water supply (Falconer 1997). This classification has been implicated in a number of poisoning incidents in Australia, including that referred to on page 398, and has attracted particular concern because it has been found in more populous temperate regions – including New Zealand, Europe, North and South America. Strangely enough, toxin production from Cylindrospermopsis is geographically determined. Australian isolates exclusively yield PSPs (paralytic shellfish poisons), while anatoxin-a (aka Very Fast Death Factor) is produced by American and European isolates (Dittmann & Wiegand 2006; Beltran & Neilan 2000). A form of this neurotoxin, anatoxin-
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Anabaena circinalis. (Courtesy: Bermuda Institute of Ocean Sciences)
a(s), is an acetylcholinesterase inhibitor, with a chemical structure similar to organophosphorus insecticides such as parathion and malathion. It is the only naturally occurring chemical of this type. Paralysis and respiratory failure are characteristic of its neurotoxicity14 (Cox 2009).
Anabaena flos-aquae, showing the curled spiral characteristic of this genus. (Courtesy: Environmental Protection Agency, US Federal Government)
Microcystis aeruginosa. (Courtesy: Kristian Peters CC-by-SA 3.0) 14 Acetylcholinesterase inhibitors have attracted interest as potential biological weapons for chemical warfare. Cyanobacteria and cyanotoxins such as anatoxin-a(s) and saxitoxin are among the newest candidates to be examined (Cox 2009).
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Some studies have indicated that a remarkably large range of cyanobacteria can produce the neurotoxin BMAA, although the actual level of the problem continues to be highly debated. It is possible that BMAA can be manufactured by all forms of cyanobacteria under the right conditions and that, because of its ubiquitous presence in the environment, low levels of exposure are normal. It may be that some individuals have an increased susceptibility, depending on genetic factors and cumulative levels of exposure (Bradley & Mash 2009; Cox 2005). A study of the potential contamination of marine organisms has confirmed the presence of BMAA in fish from the Baltic Sea (a brackish water ecosystem) and marine-dwelling molluscs from the west coast of Sweden. It appeared that there were different levels of bioaccumulation – bottom-dwelling species (turbot, fourhorn sculpin, smelt), as well as filter-feeding molluscs (mussels and oysters) contained high levels of the toxin. While BMAA was present in the muscle of tissue of some fish at low levels, fish brains (which are not usually eaten) had a much higher concentration. However, to highlight the vast differences in possible exposure, some fish species found in potential cyanobacterial bloom environments (pelagic zones) contained no BMAA. Cyanotoxins may have similar avenues of bioaccumulation that are relative to specific fish or mussel species. For instance, the hepatotoxins nodularin and microcystin can be present in high concentrations in mussels and flounder (Jonasson 2010). For this reason certain dietary preferences may present a higher risk of exposure to these toxins. The fact that BMAA is ubiquitous in the environment could be a recipe for disaster as far as neurological disorders are concerned. Researchers may well have stumbled upon one of the unknown causes of many degenerative diseases of the nervous system – and it is truly frightening to think of the implications. Recently, the possibility that BMAA exposure occurred from desert dust in Gulf War veterans hit the spotlight. Dust churned into the air during military operations was found to contain this neurotoxin, as well as the toxic BMAA metabolite DAB (diaminobutyric acid). This type of exposure could allow contact with inhalant cyanobacteria. This is not as odd as it sounds. Cyanobacterial crusts (mats) are abundant in some parts of the Gulf region.
They can be extremely large (up to 82 m2) and cover up to 56 per cent of the land area along depressions. ALS (amyotrophic lateral sclerosis) has been shown to have a higher than normal incidence among Gulf War veterans (Cox 2009; Horner 2003). A cluster of ALS cases from New Hampshire (USA), near Lake Mascoma, may also be linked to cyanobacteria (Caller 2009).
Neurotoxins and Pesticide Exposure
Insecticide spraying equipment. (Courtesy: USA CDC, Centres for Disease Control & Prevention)
In the last few decades the high incidence of Parkinson’s disease among farmers who routinely employ pesticides has led to suggestions that increasing levels of agrochemical exposure could be implicated in some way. Subsequent studies found that numerous environmental toxins can cause neurological damage. Pesticides are but one risk factor, however, for it is also possible that traumatic experiences involving brain injury can predispose an individual to the disease. These include inflammatory disorders leading to brain tissues damage, including head injuries15 or exposure to infectious agents (e.g. viral encephalitis). Athletes involved in sports such as 15 There is evidence that multiple head injuries significantly increase the risk of developing ALS (around 11-fold). This originated with a study of soccer players in Italy between 1993 and 1996 (Chen 2007). Since then numerous studies have been undertaken to evaluate the potential neurological damage, particularly involving memory, that could result from contact sports-related head injuries. Although the findings have been controversial, there does appear to be an appreciable risk with repeated injuries (Iverson 2004; Gardner 2010; Theriault 2011).
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boxing, which are associated with a high incidence of head injury, have shown a higher incidence of Parkinson’s disease – as have injured World War II veterans. There may also be a link to brain trauma in the development of memory disorders such as Alzheimer’s disease. Even soil bacteria have been implicated – studies of Nocardia asteroides exposure (injection) in rats resulted in Parkinson-like symptoms (Kohbata & Beaman 1991). Although some later investigations refuted the ability of this bacteria to cause these effects in humans (Lu 2005), Nocardia has been utilised in animal experiments for studying Parkinson’s disease (Salama & Arias-Carrion 2011). A microbe would have to cross the blood– brain barrier to cause the permanent sort of neurological damage that results in Parkinson’s disease. Exposure to chemicals is problematic for this very reason. Several classes of pesticide that can cause dopaminergic neurotoxicity (i.e. adversely affect the action of dopamine in the nervous system) are now considered potential risk factors. They include pyridinium-based agents (paraquat), dithiocarbamate-based fungicides (maneb), the insecticide rotenone, and organochlorine pesticides (dieldrin). In addition, exposure to industrial chemicals such as PCBs (polychlorinated biphenyls), manganese (which is used as the fuel additive MMT) and lead could be other serious risk factors (Gavett 2010; Landrigan 2005; Liu 2003). Certainly, this should sound warning bells with regard to infant exposure to household chemicals, particularly pesticides and insecticides with known neurotoxic effects. The increased incidence of chemically sensitive individuals should also act as a warning to the community at large of the risks we expose ourselves to on a daily basis.
Dangerous Experiments
There are many forms of neurotoxins in the environment. Aside from dietary toxins such as cyanide, which is found in Cassava and some stone-fruit seeds (e.g. peaches and apricots), there are toxins similar to the azoxyglycosides in some
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legumes (Fabaceae family). The effects of various other environmental toxins, notably pesticides, have been highly debated with regard to the level of contact and the implications for those at risk of habitual exposure. There are other chemical neurotoxins about which little is known, however. In 1983 an incident in northern California involving the use of an adulterated form of heroin by seven individuals resulted in an inadvertent neurological experiment. The unfortunate users suffered permanent neurological damage that resembled Parkinson’s disease which, luckily, responded to treatment with levodopa. Later studies in animals with MPTP (which was identified as the adulterant in the toxic heroin) showed irreversible and selective loss of dopaminergic neurons in the brain (substantia nigra). This form of damage has subsequently been used for studies of the neurological damage associated with Parkinson’s disease (Shaw & Hoglinger 2008).
Toxins from the Sea
Algal blooms, sometimes called a ‘red tide’, that are linked to cyanobacteria and dinoflagellates (a type of plankton) can involve various different toxins. This can make things quite complicated as different cyanotoxins can be produced by a single species and, conversely, individual cyanotoxins are rarely limited to a single source. Cyanobacterial blooms can thus be characterised by the presence of several different toxins. The various forms of poisoning that result from these toxic marine contaminants16 tend to fall into three main categories: • irritant effects (primarily affecting the gastrointestinal tract); • neurological damage; • hepatotoxicity (the latter can also be associated with haemorrhage and kidney damage). Low levels of some cyanobacteria (notably microcystins and nodularins) in the environment have even been implicated in an increased incidence of liver cancer 16 In addition, some toxins can persist in shellfish, remaining in the animal from several weeks to a couple of years – e.g. saxitoxin, the neurotoxin found in butterclams, can make these animals hazardous long after the toxic bloom has disappeared.
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(Cox 2009; Dittmann & Wiegand 2006). Bacterial bloom south of Fiji on 18 October 2010. Though it is impossible to identify the species from space, it is likely that the yellow-green filaments are colonies many kilometres long of Trichodesmium, a form of cyanobacteria often found in tropical waters. (Image courtesy: Norman Kuring NASA Earth Observatory)
Shellfish poisoning can present in four forms: diarrhoeal, amnesic, neurotoxic and paralytic: • The diarrhoeal form, although distressing, is selflimiting and recovery is relatively quick. The symptoms are diarrhoea, nausea, vomiting and stomach cramps. • The amnesic form, which is due to the neurological effects of domoic acid, can be quite serious. Symptoms involve gastrointestinal distress (vomiting, nausea, abdominal cramps,
haemorrhagic gastritis), headache, dizziness, visual disturbance, profuse respiratory secretions, hiccough, neurological symptoms (shortterm memory loss, brain damage, peripheral neuropathy), cardiac distress (unstable blood pressure, arrhythmia) and, occasionally, coma and death. The neurological side-effects can persist, with associated permanent short-term memory loss and neuropathy. • Neurotoxic shellfish poisoning (NSP) is due to brevitoxins from a dinoflagellate, Karenia brevis. This can result in gastrointestinal symptoms (vomiting etc.), dizziness and neurological problems (numbness and paraesthesia of mouth, fingers and toes, ataxia, slurred speech), as well as respiratory distress. This form of poisoning has been compared to a mild case of paralytic shellfish poisoning (PSP). e paralytic form of poisoning (due to PST: Th paralytic shellfish toxins) involves contact with potent neurotoxins. The most familiar is saxitoxin, which is water soluble, and heat and acid stable. This means that cooking will not inactivate the toxin. Symptoms involve gastrointestinal distress, abdominal pain, tingling and burning sensations (affecting the extremities, face and mouth), respiratory
Fishing down the food web, a North Sea perspective. (Courtesy: Hans Hillewaert, CC-by-SA 3.0)
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problems (shortness of breath, a choking feeling), confusion, slurred speech and coordination problems. Tetrodotoxin (often abbreviated TTX) is possibly the most potent neurotoxin that has been discovered from marine sources. It is certainly the best known. The name is derived from the classification of fishes (Order: Tetraodontiformes) that deploy the poison. They include pufferfish, porcupinefish, triggerfish, and the ocean sunfish (mola). However, the toxin now appears to be more widespread among marine life than was first thought. It has also been found in the Blueringed Octopus and the Rough-skinned Newt, a fresh water denizen – as well as various starfish, crabs, seaslugs, ribbonworms and arrow-worms. The method of toxin production has an intriguing link with symbiotic bacteria in these animals. TTX has pharmaceutical attributes – originally deployed in Japan in the 1930s, it has proved useful for the treatment of serious pain (terminal cancer, migraine) and to mitigate the agony of heroin withdrawal (Hagen 2008; Stimmel 2002).
Pufferfish, Arothron hispidus. (Courtesy: Mila Zinkova)
While TTX is highly poisonous, the level at which it is present can vary greatly. Exposure may not always be fatal. The fact that near-lethal doses can result in a death-like state has led to a certain level of infamy for the poison. It was a proposed ingredient in Haitian voodoo rituals, with the purported ability to induce a state resembling zombieism. In 1983 the ethnobotanist Wade Davis popularised this idea – although it was later discarded. Descriptions of so-called ‘voodoo zombies’ did not correlate well with that of TTX poisoning (Hines 2008; Anderson 1988). Other than
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experiments involving this misguided use in Haiti, most reports of poisoning originate from Japan, where pufferfish (fugu) is a traditional delicacy. It is served in special restaurants, prepared by highly trained chefs who are a very familiar with removing the toxic fish parts. Formal dining casualties are rare, although incidents still occur among fishermen who carelessly prepare their catch. There are a couple of reports that mention dogs being poisoned by pufferfish and seaslugs in New Zealand (The New Zealand Herald 2009; McNabb 2009). Other fishing sites for pufferfish include the Atlantic Ocean, the Gulf of Mexico and the Gulf of California.
Ciguatera Ciguatera poisoning was first described in 1774 by William Anderson, surgeon’s mate, on the voyage of HMS Resolution (1772–75). It is a fairly common form of fish poisoning in northern Australia, throughout the Pacific Islands and the Caribbean. It is due to the bioaccumulation of toxins (ciguatoxin, maitotoxin, scaritoxin, palytoxin) in over 400 species of tropical reef fish that dine on the dinoflagellate Gambierdiscus toxicus. These are heat-resistant toxins that cannot be detoxified by normal cooking processes. The symptoms are gastrointestinal (nausea, vomiting, diarrhoea), followed by aches and pains (headache, muscle aches) and neurological problems (paraesthesia, numbness, ataxia, hallucinations). The toxin can cause sexual discomfort (pain on intercourse) suggesting its sexual transmission, and it may also be transmitted in breast milk. The effects of ciguatera poisoning can persist for a long time (from two months up to 20 years). It is well known as a ‘relapsing illness’ that can be precipitated by fish and fish-containing products – as well as some other odd triggers such as alcohol, chemical fumes (including bleach), chicken, eggs and nuts. There is no effective antidote and treatment is symptomatic. There are diverse traditional herbal remedies for the condition about which very little is known and, unfortunately, virtually no research has been undertaken.
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Dietary Neurotoxins Guadeloupean Parkinsonism
Flower and immature fruit of the Soursop, Annona muricata.
In the late 1990s a condition named Guadeloupean Parkinsonism was identified in the West Indies. It closely resembled the neurological disorder described in Guam (see page 367) and a link to a dietary component was suspected. However, the symptoms differed in some very specific ways, some of which made the condition highly distressing. In a study of 160 patients it was found that symptoms were distinguished by a high level of dementia (92%), a high frequency of tremors (>50%), dysautonomia (disorders of the autonomic nervous system, 50%), hallucinations (59%), and a form of the disorder the resulted in oculomotor (eye movement) dysfunction. There was also resistance to treatment with levodopa, a dopamine-replacement drug that is normally used to treat Parkinson’s disease (Lannuzel 2007). Early investigations suggested a tentative association between the use of herbal teas or fruit from locally-grown Pawpaw (Asimina species) or Soursop (Annona muricata). These are members of the tropical Custard Apple family (the Annonaceae) which, surprisingly enough for a popular tropical fruit resosurce, can have toxic potential. The seeds can be highly poisonous, and have long been utilised as a source of insecticides – although there are other parts of the plants (leaves, roots) with medicinal uses that may
contain similar toxins. Acetogenins have been the primary suspects, particularly annonacin from the Soursop, although Pawpaw pulp also contains these compounds (asimicin, bullatacin, bullatalicin)17 (Pomper 2009; Lannuzel 2003; Caparros-Lefebvre 2002; Caparros-Lefebvre & Elbaz 1998; Roman 1998). Examination of extracts (root-bark, fruit) prepared from the Soursop (Annona muricata) confirmed that neurodegenerative effects were linked to the alkaloid constituents. The level of exposure can vary: a cup of tea contains fairly low levels of annonacin (decoction/infusion of the leaf: 140 mcg), and the average Soursop fruit contains 15 mg, while the levels in a can of nectar are much higher (36 mg). However, it is estimated that eating a single fruit or a can of nectar daily for a year would provide the equivalent to the amount of annonacin that causes brain lesions in rats. There are other neurotoxic acetogenins in Soursop fruit – reticuline and N-methylcoculaurine (Lannuzel 2006, 2002; Champy 2005, 2004; Kotake 2004). It is worrying this type of neurological condition may be more widespread than initially thought. Annonaceae fruit consumption (particularly Soursop) has been implicated in atypical Parkinsonism in New Caledonia, and a Londonbased study of African-Caribbean and Indian communities has suggested the presence of a similar neurological disorder (Angibaud 2004;
Asimina triloba is known as the North American Pawpaw Tree, while the Long-leaf Pawpaw refers to Asimina longifolia. This genus is not related to the tropical Asian Pawpaw, Carica papaya. (Image courtesy: Scott Bauer, USDA, Agricultural Research Service) 17 It is possible that sterol glucosides (or similar components) may also be involved. The acetogenin reticuline has a structural similarity to sterol glucosides (Shaw & Hoglinger 2008).
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Hu 2002). Equally worrying is the finding that animal studies have indicated systemic exposure to rotenone produces a pattern of neurological damage similar to that of the acetogenins (Shaw & Hoglinger 2008).
Yellow-billed Cuckoo with Asimina triloba fruit, from The Birds of America by the naturalist and painter John James Audubon. This work was first published in seven volumes between 1827 and 1838, in Edinburgh and London.
There is another link between plant-based neurotoxic chemicals that should be mentioned. The excessive consumption of drought-resistant legumes in a number of countries has been linked to the development of a degenerative neurological condition known as lathyrism. There have been episodic outbreaks in India, Ethiopia and Bangladesh. The main culprit is Lathyrus sativus (the Grass Pea, Chickling Pea/Vetch or Kesari), although L. cicera and L. clymenum have also been implicated. Small amounts of these pulses cause no untoward problem, as they are quickly metabolised and excreted in the urine. However, toxic effects manifest if their proportion in the diet increases (to 30–50%) and their use is prolonged (more than three months). Lathyrism is an extremely debilitating disorder characterised by muscle twitching. It begins with initial symptoms of leg stiffness that develop into exaggerated knee- and ankle-jerk reflexes. Untreated, it can progress to irreversible spastic paralysis of the legs, memory loss, arthritic pain (arthralgia), gastrointestinal distress, and urinary and sexual dysfunction. The condition is due to spinal lesions that are induced by the neurotoxin
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BOAA (β-N-oxalylamino-L-alanine) (Bell & Nunn 1988). The emotional and social consequences of lathryism are tragic. Generally, the victims become ostracised, with a complete loss of social standing. Many end up as beggars, living a miserable life on the streets.
Lathyrus sativus flower.
There is a structural similarity between the Cycad toxin BMAA and the Grass Pea neurotoxin BOAA (=ODAP i.e. 3-N-oxalyl-L-2,3-diaminopropionic acid). However, the toxicity of the Grass Pea depends on the variety, season and growing conditions.18 The average concentration of β-ODAP in ripe seeds is less than 1 per cent, although seedlings (which are not eaten) can contain a higher concentration. The toxin is water soluble and prolonged cooking converts it to a much less toxic form (α-ODAP). This means that boiled snacks and Grass Pea flour tend to have a substantially lower toxic potential. However, roasted products retain their toxicity, and this can include many bread-based staple dietary items. Steeping the seeds for three minutes will remove around 30 per cent of the toxin, although this level can still pose a risk. The best method of detoxification is to remove the seed husk and boil for several hours, discarding the water, which eliminates 70–80 per cent of the toxin (seeds contain 282–810 mg/100 g dry seeds, average 455 mg β-ODAP). However, water can be a scarce commodity in the countries where the Grass Pea is consumed. 18 The concentrations of BOAA in Lathyrus sativus and L. ochus are 4–5 times higher than in L. cicera (Aletor 1994).
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Lathyrus sativus seeds. (Courtesy: Steve Hurst @ USDANRCS PLANTS Database)
Grass Pea, Chickling Vetch, Indian Pea or Kesari (Lathyrus sativus), from William Curtis, The Botanical Magazine, Vol. 4, 1790.
Indeed, there is a higher incidence of poisoning during times of drought (Barceloux 2008). Studies continue to examine the poisonous potential of the Grass Pea with the aim of producing cultivars of Lathyrus sativus and L. cicera that contain low levels of the toxic compounds (as well as their chemical precursors). This has the potential to make the crop a significantly safer and viable food source for poor countries. The toxin BOAA can be found in other genera of the Fabaceae (Leguminosae) – notably species of Crotalaria and Acacia. An early study in 1977, which analysed the seeds of more than 250 genera of Legumes, determined that the toxin was present in 13 species of Crotalaria and 17 species of Acacia (Qureshi 1977). There are also a number of Australian
Macrozamia moorei in the Botanical Garden, Palermo. (Courtesy Tato Grassi: Wikipedia)
Crotalaria species that contain pyrrolizidine alkaloids – plant toxins that can be strongly associated with the development of liver failure (veno-occlusive liver
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Macrozamia moorei, male cone. In a somewhat surprising turn of events, BOAA has been identified in the seeds of the Queensland Cycad Macrozamia moorei, and in the seeds of M. communis from New South Wales (Pan 1997). (Image courtesy Tato Grassi: Wikipedia)
disease) and liver cancer in animals and humans.19 Of these, the weedy Crotalaria spectabilis, which is naturalised in north Queensland and the Northern Territory, contains moderate alkaloid levels – as does C. mitchellii, which is abundant throughout New South Wales and Queensland. Various other poisonous natives contain higher levels, including C. crispata, C. novae-hollandiae subsp. novae-hollandiae (chemotype 2), C. ramosissima and C. retusa var. retusa. Recently, a local variant of the Trefaoil Rattlepod (Crotalaria medicaginea, chemotype cromedine) from centralwestern Queensland has been involved in a horsepoisoning incident linked to hepatotoxicity. However, Crotalaria goreensis, C. aridicola subsp. densifolia and C. medicaginea var. neglecta do not have hepatotoxic properties (Fletcher 2009 & 2011). Monocrotaline is one of the highly toxic pyrrolizidine alkaloids of part-icular interest that is present in a number of species, including the New Holland Rattlepod (Crotalaria novae hollandiae subsp. hollandiae, chemotype 2), the Showy Rattlepod (C. spectabilis) and the Wedge-leaf Rattlepod (C. retusa). In addition to causing liver dysfunction, monocrotaline has been linked to neurological damage in the central nervous system. It has also been used to induce pulmonary hypertension in experimental animal studies (Pitanga 2011). 19 Around 600 pyrrolizidine alkaloids (and their N-oxide) have been identified in over 6,000 different plants – although not all are poisonous, as only around half of these compounds have heptotoxic potential. While these alkaloids are prevalent in some genera of the Fabaceae family, toxic pyrrolizidine alkaloids have also been isolated from a number of other plant families – the Boraginaceae, Asteraceae (Compositae) and Orchidaceae (orchids), and occasionally from Poaceae (grasses) and Convolvulaceae (bindweeds) (see Smith & Culvenor 1981 for further details).
Numerous Crotalaria species produce typical pea-like yellow flowers that are difficult to tell apart. The seeds, which detach within the seed pod when ripe, have resulted in the common name ‘Rattlepod’ being applied to many species – of which there are 41 in Australia (a number of which are naturalised).
The Streaked Rattle-pod, Crotalaria pallida, is one of the naturalised species in the northern Australian tropics that contains ODAP (Quereshi 1977).
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The infamous Chillagoe Horse Poison (Crotalaria aridicola), which is found throughout northern Australia, is so named because incidents of poisoning usually involve horses, which tend to develop a liking for the plant (Everist 1981). While the toxic component remains a bit of a mystery, the horses develop oesophageal ulceration and blockage with a resultant inability to swallow food or water. They soon experience rapid weight loss, quickly become emaciated and die. The Trefoil Rattlepod has been linked to similar incidents (Dowling & McKenzie 1993).
Seed pods of Lathyrus odoratus.
to fame. In the 1800s the Czech monk Gregor The Lathyrus Peas Mendel famously The Lathyrus Peas are closely allied to the Garden Peas used pea plants (Pisum) and the Vetches (Vicia), all of which belong in some of his to the Broad Bean family (Fabaceae). The Lathyrus experiments on genus contains over 100 species, some of which have hybridisation. In distinctive characteristics, both good and bad. While the early twentsome species in Lathyrus are edible, most are not and ieth century, it appears wise to avoid experimentation. A notable Britain’s Regexception is the tuber of the small climbing perennial inald Punnett Sweet Pea flowers. (Courtesy: expanded Lathyrus tuberosus, which was widely consumed this Amanda Wray) in Europe before the Potato arrived from South work and many America. genetic principles The most famous of the Lathyrus genus is the were discovered or confirmed in Sweet Pea studies Italian Sweet Pea (L. odoratus) – a species prized – trials that led to a greater understanding of in seventeenth and eighteenth century Europe for inherited traits in plants and establishment of the its remarkably sweet perfume. From these origins laws of heredity. From these origins the modern many colourful cultivated forms were developed. science of genetics was to eventually emerge. The Sweet Pea has a significant historic claim Although the fruit of the Sweet Pea is rarely eaten, the plant has been linked to a form of lathyrism known as Sweet Pea lathyrism, odoratism or osteolathryism – which is more common in animals than humans. This is due to β-aminopropionitrile (BAPN), a lathyrogen that differs from the neurotoxin ODAP (BOAA). The condition affects the linking of collagen (a connective tissue protein) resulting in defective skin ageing, hernias, aortic Thanks to the Chickling, by Spanish artist Francisco Goya (Gracias á la almorta) 1810–14. aneurysm and skeletal deformities Excessive consumption of sweet peas, known as chicklings, resulted in lathyrism, with (Barceloux 2008). One study of permanent crippling of the legs.
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500 individuals with neurolathyrism in Bangladesh identified 60 cases of osteolathyrism – all of whom had not only eaten the seeds, but also utilised the green parts of Lathyrus sativus. The plant (leafy parts) contains a compound (2-cyanoethylisoxazolin-5-one) which can produce BAPN, thereby resulting in this uncommon condition (Haque 1997).
A number of ornamental Lathyrus ‘peas’ have been adopted into cultivation in Australian gardens. These include the ornamental vine-like Wild or Two-flowered Pea (Lathyrus grandiflorus), the European Mountain Pea (L. montanus), and the Everlasting Pea (L. sylvestris) – as well as the Chilean Perennial Pea (L. latifolius) and Blue Perennial Pea (L. pubescens). All are suspected of being toxic, some more so than others. In particular, children should be kept away from experimenting with their seeds (Wilson 1997). Species listed as weeds in Australia include the Perennial and Everlasting Peas, the Sweet Pea (Lathyrus odoratus), the Slender Wild Pea (L. sphaericus), the Tangier Pea (L. tingitanus) and the Angular Pea (L. angulatus) (Lazarides 1997).
Bitter Black Vetch (Lathyrus niger). The small black seeds of this species should not be confused with the edible Black Pea (Pisum sativum), despite the fact that the same common name may be used for both plants. Bitter Black Vetch produces tiny black seeds that have a high neurotoxin content.
Favism from Broad Beans
Wild Pea or Two-flowered Pea (Lathyrus grandiflorus).
Chilean Perennial Pea (Lathyrus latifolius).
Dried broad beans.
Broad beans in pod. (Courtesy: Rasbak, Wikimedia Commons Project)
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convicine, isouramil), particularly if they are raw or undercooked. Even inhaling the pollen can provoke life-threatening incidents. The severity of the reaction, which can vary greatly, is not only influenced by variations in the toxic components present – there are environmental conditions that may act as a chemical trigger. In severe cases, the anaemia can be associated with jaundice, dark or blood-stained urine, and collapse. Favism involves a hereditary male sex-linked deficiency of the enzyme glucose-6-phosphate dehydrogenase (G6PD). Its highest incidence is in the Mediterranean region (particularly in Sardinia), although it is also found in individuals of African, Middle Eastern and Southeast Asian origins (Cooper & Johnson 1984). There is, however, one interesting benefit for sufferers – they have a good degree of immunity to malaria. The parasite that causes malaria appears to be rapidly cleared from the system through the spleen and is thus unable to cause long-term damage.
Vicia faba, from Flora von Deutschland, Österreich und der Schweiz, by Professor Dr Otto Wilhelm Thomé, Gera, Germany, 1885.
The Broad Bean (Vicia faba) has been a crop resource around the Mediterranean since prehistoric times, and the large seeds were also added to animal feed. In Australia Vicia faba is cultivated for human consumption, and the Tick Bean (V. faba var. minor), Horse Bean (V. faba var. equina), V. faba var. major and Spurred Vetch (V. monantha) for animal fodder. The Broad Bean, although not normally considered poisonous, has been associated with an inherited disorder known as favism (fabism, fabismus) which can cause the development of haemolytic anaemia (excessive destruction or haemolysis of red blood cells). Other symptoms of exposure include vomiting, abdominal pain, dizziness and raised temperature. Susceptible individuals experience reactions when exposed to Broad Beans (which contain vicine, divicine,
Prunus and Manihot: Cyanide Poisoning
There is one other plant-derived neurotoxin, cyanide, that is appropriate for inclusion in this discussion. In 1871 Dr George Bennett commented on the similarity of a number of toxins and their associated detoxification strategies: An acrid or irritating poison evidently exists in the seeds of the Macrozamia: this property may be in the epidermis of the seed as in those of the castor oil tree [Ricinus communis], or it may be contained in the seed itself having a deleterious alkaloid the precise nature of which can only be ascertained by careful analysis. It has been found that when the seed in a fresh state had been cut up and given to fowls it has been generally fatal to them. The starch prepared from Macrozamia would, no doubt, prove as a commercial article as valuable as that procured from the Manihot (Jatropha manihot) which forms the cassava bread and also tapioca. The juice of the Manihot is acrid and poisonous, owing, it is said, to the presence of hydrocyanic acid [cyanide], and probably also to an acrid principle, and contains more active poisonous properties
NEUROTOXINS: PLANTS OF PERILOUS CONSEQUENCE than … Macrozamia. The cassava is made by grating fresh roots, squeezing out the juice, and then baking into cakes on an iron plate, this process I have seen used at the Mauritius some years since, when the Manihot was extensively cultivated as food for the slaves. The Tapioca is prepared, by beating the root into a pulp, washing it with cold water, and then allowing the fecula to subside from the milky fluid which flows from it; being then dried on heated plates, it becomes of a granular form. By the washing and heating, similar to the starch of Macrozamia, the poisonous matter being both soluble and volatile, is dissipated (Bennett 1871).
Cassava Preparation The preparation of the cyanide-containing Cassava root is extremely important; the guidelines must be followed exactly to allow the safe use of this vegetable in the diet. Cooking alone is generally insufficient to remove all the cyanide. The root must be peeled and the leaves chopped, then both washed thoroughly before being cooked. These physical actions damage the plant tissue, liberating an enzyme (linamarase) that initiates the decomposition of cyanide (primarily from linamarin). Ultimately, hydrogen cyanide (HCN) is formed. This is a volatile gas that readily dissipates during drying or roasting. Fermentation is an equally effective detoxification process. Properly prepared Cassava, when combined with other foods in the diet, is associated with a low incidence Cassava roots. of poisoning – although the risk of cyanide exposure from long-term inadequate preparation cannot be ignored. Chronic exposure can result in problems such as ataxic neuropathy, calcific pancreatitis, goitre, cretinism, and possibly diabetes (Cliff 1985; Assan 1984; Lancaster & Brooks 1983).
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Cassava (Manihot esculenta) is a tropical crop with the potential to cause a neurotoxic condition that resembles lathyrism. This disease, known as konzo, has similar symptoms involving the development of persistent spastic weakness of the legs and nervous system degeneration. The disorder has a higher frequency of occurrence in African communities that rely on Cassava roots as part of their diet. Outbreaks are associated with an increased intake of a cyanideliberating glycoside (linamarin20), particularly in protein-starved individuals. Thiocyanate, which is the principal metabolite of cyanide, appears to be the culprit responsible for the neurological damage (Ludolph & Spencer 1996; Omelchenko 1999; Spencer 1999; Tor-Agbidye 1999). There is also a slow-developing form of nerve damage called tropical ataxic neuropathy that has been linked to a diet largely composed of Cassava, although the complete cause remains unknown. The condition differs in that it is a chronic disorder with cyanide levels much lower than those found in konzo patients (which are 20 times higher). In addition, where dietary iodine levels are low, Cassava consumption can aggravate goitre and cretinism. Thiocyanate, which is normally removed in the urine, is a goitrogen (that is, it inhibits the uptake of iodine by the thyroid gland).
The leaves of Manihot or Cassava.
The role of Cassava in cyanide poisoning has long been known to the medical world. The following summary of the effects of acute poisoning was provided by Torald Sollmann (1949): Hydrocyanic (prussic) acid is perhaps the most rapidly acting poison. It produces death with asphyxial symptoms 20 The cyanogenic compounds linamarin and lotaustralin can form HCN, an action that is initiated by the enzymatic action of the linamarase.
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons Cross-section of Manihot utilissima root. In northern Queensland the introduced Manihot utilissima (known as Cassava or Tapioca) has been used by Aboriginal communities for treating gastrointestinal distress. The roots were scraped and the milk exudate drunk as a remedy for diarrhoea or belly-ache (Kyriazis nd).
by hindering the oxidative processes of the tissues. It also interferes with most catalytic reactions and is therefore a general protoplasmic poison. Compounds containing the CN radical are toxic only if they can liberate HCN. Occurrence: Hydrocyanic acid exists in glycosidal form as amygdalin in many plants, especially in the seeds and leaves of the cherry, almond, peach, and so on. This amygdalin, when pure, is almost entirely harmless, except as it is decomposed by the body.21 But in most plants it coexists with the ferment emulsion, by which it is split up in the presence of water into hydrocyanic acid, glucose and benzaldehyde. One Gm. of cherry kernels yields 1.7 mg. of hydrocyanic acid; 1 Gm. of bitter almond pulp yields 2.5 mg of hydrocyanic acid. The ancient Egyptians are said to have prepared it as a poisonous extract from the peach and other plants, and the Russians used these as a suicide poison (Sollmann 1949).
Hydrocyanic acid gas was once used as a method of fumigating food, and for household pest control. It effectively killed everything from cockroaches to rats and, none too surprisingly, was responsible for numerous cases of accidental poisoning: Hydrocyanic acid is rarely used in criminal poisoning (0.5 per cent of the recorded cases), because its quick action leads to the detection of the crime; but cyanides are often employed in suicide. Death is prompt and practically certain in spite of any treatment, if enough has been taken. Potassium cyanide can be easily obtained through its technical uses in photography, electroplating, 21 Amygdalin has also been referred to as vitamin B17, and was formerly thought to be the same as laetrile (laevorotatory nitriloside). However, the latter compound was shown to have a chemical structure different from amygdalin (Fukuda 2003).
cleaning of metals. Many fatal accidents have occurred from fumigations with the gaseous acid. Pure hydrocyanic acid is very volatile and toxic. Sheele, who discovered hydrocyanic acid, was killed by the vapors set free in the breaking of a flask of this fluid (Sollmann 1949).
The onset of unconsciousness is rapid and, in severe poisoning, death can occur within 2–5 minutes. Mortality on exposure is high (around 95%), with most fatalities resulting in 15–60 minutes – although if a person survives the first hour they are likely to recover. The Brown Rat (Rattus norvegicus). Hydrocyanic acid was once used to kill vermin that ranged ‘from rats to roaches … It is also extensively used for fumigating food, as well as other goods, and houses. It is safe if it is properly applied and followed by a thorough airing … It is not injurious to most goods; it is not corrosive, and a concentration that kills rats does not injure tea or tobacco … It penetrates readily, so that weevils in the centre of a car of flour are killed by six hours’ exposure … The objectionable feature is liability to accidental poisoning’ (Sollmann 1949). Enough said, really. (Image courtesy: U.S. Federal Parks Service).
Australian Swamp Rat (Rattus lutreolus), from John Gould, FRS, Mammals of Australia, Vol. III, Plate 12, London, 1863. This is a vegetarian native rodent found in low lying wetlands and swamps. It is native to eastern Australia (Fraser Island in Queensland, ranging to New South Wales and Victoria), South Australia and Tasmania. An outlying population is also found at Atherton, in northern Queensland.
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Potassium cyanide (KCN) is a highly toxic compound that is used in mining ventures for gold extraction, for photography, electroplating, jewellery manufacturing and cleaning. It is also the toxin used by entomologists to kill insects for preservation and study. The poisonous effects of potassium and sodium cyanide are identical. (Image on left courtesy: Morienus, CC-by-SA 3.0, unported; image on right courtesy: www.SureCureAntiques.com)
Cyanide in Seeds: The Rosaceae
The Rosaceae family is a classic cyanide-containing plant classification. The Peach (Prunus persica), Plum (P. domestica), Apricot (P. armeniaca), Cherry Laurel (P. laurocerasus) and Bitter Almond (P. dulcis var. amara) all belong to this family. There are just two native Australian species, one of which has been utilised as a food resource by Aboriginal people. This is the tropical Queensland rainforest tree known as Almond Bark, Prunus turneriana, whose distribution extends from northern Queensland to Papua New Guinea.22 In general the fruit was regarded as inedible and the seed toxic. Nevertheless, the explorer Christie Palmerston recorded its use by his Aboriginal guides: Returned to camp where Willie had a lot of meal crushed for me to make Johnny-cakes from the ‘Too-moo’ nut [Prunus turneriana, Wild Almond] so named by the aborigines. The fruit is similar to a small black plum. A heap of them are placed in a hollow rock in which water is poured, then the fruit is tramped off, next divested of its shell, then crushed into meal with two stones, a flat one on the ground; the other, a small round one, kept in the hand. The meal is then placed between two frond-like leaves, and toasted on the coals like Johnny-cakes. The fruit adheres to the nut which has a wrinkled surface. This fruit also contains evil properties, and requires soaking in water four or five hours after it is crushed (Savage 1989).
There are only two native species of Prunus found in Australia: Prunus turneriana (syn. Pygeum turnerianum), or Almond Bark, the fruit of which is illustrated here, and P. brachystachya. However, quite a number of species have been listed as naturalised: Prunus armeniaca, P. avium, P. campanulata, P. cerasifera, P. cerasus, P. domestica, P. dulcis, P. laurocerasus, P. lusitanica, P. mahaleb, P. munsoniana, P. persica and P. salicina.
When the seed is cut, like many in the genus, it has the aroma of almonds. The cut bark and broken twigs emit a similar fragrance – hence the name of the tree. In Australia the fresh kernels of the fruit were used as an analgesic remedy for toothache, ground and applied to the area. 22 The introduced Prunus grisea var. grisea is also found in northern Queensland.
Cyanide Toxin Sources Poisoning due to large amounts of HCNcontaining seeds or kernels has been recorded from a range of edible fruits: Bitter Almonds (Prunus amygdalus), Peach (P. persica seeds), Apricot (P. armeniaca kernels) and Apple (Malus
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Nectarine, the smoothskinned form of Prunus Apricot, Prunus armeniaca. persica.
pumila pips). Plum stones (Prunus domestica) contain cyanogenetic glycosides (around 2.5%) – cyanide-yielding toxins (i.e. amygdalin, prunasin, linamarin, lotaustralin, triglochinin) that are widespread in the Rosaceae family. In particular, the leaves of the Prunus genus, which have been eaten by some animals, can contain HCN at levels that risk livestock poisoning (around 0.02% HCN). Cyanide poisoning of livestock has occurred from the North American Wild Black Cherry (Prunus serotina) and Chokecherry (P. virginiana). These species have a high content of prunasin, with larger concentrations occurring during dry years. Fresh leaf samples of other species may have a wide range of HCN values (0.1% HCN = approx. 100 mg HCN/100 g fresh leaf ). Values (per 100g) according to Duke (1985): • Apricot, Prunus armeniaca: 275 mg23 • Rocky Mountain Chokecherry, Prunus melanocarpa [P. virginiana var. melanocarpa]: 368 mg • Cherry Laurel, Prunus laurocerasus: 100 mg • Bird Cherry, Prunus pensylvanica: 91 mg (wilted leaf 143 mg) • Peach, Prunus persica: 66 mg (peach pits 164 mg) • North American Wild Black Cherry, Prunus serotina: 212 mg • Chokecherry, Prunus virginiana: 143 mg (wilted leaf 243 mg). 23 Cases of poisoning by Apricot stones in children have been reported. Cultivars with sweet seeds have a low level of cyanogenetic glycosides (e.g. 11.7 mg/100 g), in comparison to bitter-tasting seeds (130–180 mg/100 g) (Frohne & Pfander 1984).
The Plum, domestica.
Prunus
HCN values according to Duke (1994):
• Almond, Prunus dulcis: 70,000 ppm (seed) • Black or Wild Cherry, Prunus serotina subsp. serotina: 2,500 ppm (leaf ) • Cherry Laurel, Prunus laurocerasus: 1,200 ppm (leaf ); 340 ppm (seed) • Plum, Prunus domestica: 500 ppm (seed) • Cassava, Manihot esculenta: 1,800 ppm (leaf )
There are a couple of additional points that deserve mention when dealing with the Rosaceae. Many Prunus species contain the toxin amygdalin – the chemical breakdown of which leads to the formation of the cyanide-based compound hydrocyanic acid, as well as benzoic aldehyde and glucose. Amygdalin can be present in relatively high amounts (up to 8%) in Apricot kernels, although wild varieties can contain more than 20 times the level found the cultivated Apricot (Frohne & Pfander 1984). Bitter Almond (Prunus amygdalus) is equally toxic. A dozen untreated seeds can result in poisoning – vomiting, abdominal pain, pulmonary oedema, lactic acidosis and coma (Barceloux 2008). The figures below provide an indication of the variation of amygdalin in some common fruits (species and % amygdalin) (Frohne & Pfander 1984): • Bitter Almond (Prunus dulcis var. amara): seeds 5% • Apricot (Prunus armeniaca): seeds up to 8%
NEUROTOXINS: PLANTS OF PERILOUS CONSEQUENCE • Plum or Damson (Prunus domestica): seeds up to 2.5% • Peach (Prunus persica): seeds up to 6%.
Bitter Almond: flowers and fruit, from Koehler’s Medicinal Plants, 1887.
Peach Kernels, a Traditional Chinese Herb
Peach kernels prepared for use in the Chinese remedy Tao Ren.
Peach kernels have been utilised in traditional Chinese medicine. Tao Ren (sourced from Prunus persica, and P. persica var. davidiana) and Ying
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Ren (sourced from P. armeniaca, P. armeniaca var. ansu, P. mandshurica, or P. sibirica) have provided antitussive and anti-asthmatic remedies useful for the treatment of cough, asthma, acute or chronic bronchitis. In addition, Tao Ren has been highly regarded as a remedy for ‘blood-stasis’ that was particularly useful for treating injuries (bruising, traumatic pain) characterised by blood ‘congestion’, including menstrual disorders (amenorrhoea, dysmenorrhoea). A couple of additional recommendations include its use for febrile conditions (malaria), and for alleviating constipation in aged or debilitated individuals (acting to moisten and lubricate the intestines) (Bensky & Gamble 1986; Yeung 1985). Interestingly, Tao Ren has shown therapeutic potential for the cardiovascular system and Peach kernels have been utilised in the treatment of hypertension. In Korean medicine Prunus persica var. davidiana has also been utilised for painful conditions such as neuritis and rheumatism. Investigations have shown that a stem extract demonstrated cholesterol-lowering actions and blood sugar lowering (hypoglycaemic) activity in animals. The effects of this flavonoid-containing remedy were linked to a flavanone (prunin) – which has also been isolated from a number of other useful herbs, among them Cochlospermum gillivraei, Miscanthus sinensis and Acacia farnesiana (Choi 1991a, 1991b). Tao Ren contains cyanogenetic glycosides including amygdalin (2.3–3.7%) and prunasin (0.38%). Dan Bensky and Andrew Gamble (1986) note that overdoses of the herb can result in dizziness, nausea, vomiting, and headache, which can progress to dyspnoea, spasms, dilated pupils, arrhythmia and coma. The lethal dose is around 50– 60 kernels for adults and 10 kernels for children. Overdoses were generally treated with activated charcoal and syrup of ipecac, although the latter has fallen from favour in conventional medicine. In Chinese traditions, Apricot tree bark or the root cortex were used as antidotes. Detoxification processes involve cooking (stir-frying or steaming the seed), removal of the outer seed coat, and combination with sugar (Yeung 1985; Yen 1992).
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Peach flowers have been used as a diuretic for treating anuria and dropsy, as well as having sedative attributes. The remedy was also employed for treating skin disorders including acne and favus24 – and as a vermifuge for worm infestations. The leaf has been similarly utilised as an antiparasitic, as well as having astringent and febrifugal properties that were considered valuable for treating cholera and typhoid (Duke & Ayensu 1985). (Image courtesy: flagstaffotos.com.au, CC-by-SA 3.0)
24 Favus is an odd type of fungal infection due to Trichophyton schoenleinii – which causes the skin to acquire a crust-forming scabby appearance, particularly on the scalp. It can be quite disfiguring and, in the past, individuals suffering from favus were sometimes mistaken for lepers, and similarly incarcerated. Fortunately, today the condition is easily treated by the antifungal drug griseofulvin.
The Forest Apothecary, original artwork Lolli Forden. The sheer vitality and extraordinarily rich floral resources of the Australian forest continue to intrigue and tantalise the scientist. Medicinal plants have been the mainstay of therapy since time immemorial, and a number of highly important drug plants of value for anaesthesia and surgery originated from the tropical jungles – a truly awe-inspiring and remarkable environment that today needs protection across the world.
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Laetrile: The Anticancer Drug
The theory behind the once heavily-promoted anticancer product Laetrile, which came to public notice in the early 1950s, was based on the cyanogenic properties of amygdalin. The idea was that because cyanide (hydrocyanic or prussic acid) causes asphyxiation, even in very small doses, cancer cells might likewise die if subjected to a lack of oxygen. The trick was to get the cyanide into the cancer cell. The mechanism of action was based on the enzyme β-glucosidase. This enzyme, which is found in tumour cells, could hydrolyse amygdalin and release the toxic cyanide which would, in turn, be taken up by the cancer cell. The activity of β-glucosidase was thought to be greater in the cancer cell (in comparison to normal body tissue) which thus would have less capacity to detoxify the cyanide. However, amygdalin did not show antitumour activity in animal experiments (Weiss 1988). Laetrile, however, is not amygdalin. Extracts of Bitter Almond contain plant enzymes that liberate cyanide (as hydrocyanide, HCN) – but laetrile (D-amygdalin) is a semi-synthetic compound that does not contain these enzymes. Therefore intravenous administration would not produce cyanide poisoning (Barceloux 2008). A great
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deal of controversy erupted over the issue. Ultimately Laetrile was banned in the USA in 1971. A review of the situation took place in 1980 with a clinical study that, unfortunately, showed no benefit from the treatment. Indeed, Steve McQueen was one of a number of famous people who died despite its use. Even so, Laetrile continues to be proposed as an anti-cancer treatment and there are many anecdotal reports that attest to its effectiveness (Weiss 1988; Duke 1985). There is, however, another chemical complication that should be taken into consideration. The addition of vitamin C potentially increases the conversion of amygdalin to cyanide by reducing the detoxification effect of cysteine. The combination of amygdalin with vitamin C can therefore result in severe cyanide poisoning (Barceloux 2008). Those who think of eating crushed Peach or Apricot pits, or Bitter Almond seeds, as an alternative to Laetrile are simply asking for trouble. There are numerous reports of serious cases of cyanide poisoning due to eating Apricot seeds. Accidents can happen easily and many cases have involved children (Weiss 1988; Duke 1985). Indeed, the ancient Egyptians used amygdalin poisoning as a method of capital punishment – it was known as the ‘penalty of the peach’.
• The fact that plants can have a profound effect on neurological function has inspired the development of a number of drugs that have become indispensable in modern medicine, notably analgesics, muscle relaxants, anaesthetics, cardiotonics and antihypertensives – some of which remain in use today in one form or another. Importantly, a number of herbs have yielded compounds that support brain function. A few, such as the small weedy Gotu Kola and Brahmi, have an ancient history of use as memory restorative agents – a tradition that has been extremely well supported by modern studies. The next volume, An Antipodean Apothecary, not only examines these topics, it also takes a look at the medicinal traditions that were imported with the first colonists to Australia – and the somewhat remarkable level of validation that has been provided by subsequent studies. Once again, we take a journey through our past into a new and intriguing future for medicinal plants. Natural products have played a pivotal role in the development
of antibacterial drugs – an important issue in an era that has recently seen the evolution of numerous forms of drug-resistant microbes. It may come as a surprise to learn that a number of native plants have excellent antimicrobial potential that has already been established by investigators. The Australian flora is a resource that has been tapped into in the past, quite successfully, for the development of drugs that were considered indispensable during the war years – a time of international shortages of various essential medicines. Surprisingly, some of the compounds discovered continue to be the basis of drug supplies today. The commercial development of the contraceptive pill also has origins within the Australian Solanaceae. These topics present an opportunity acquire a greater appreciation of the bountiful flora that resides on our own doorstep. Certainly, the plants on this ancient continent continue to present innumerable opportunities for discovery.
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INDEX A α-amylase 22 α-carotene 144, 146, 147 α-chaconine 150, 151, 152, 153, 155 α-mannosidase 21 α-naphthoquinone 239 α-pinene 38 α-solanine 150, 151, 152, 154, 155 α-tocopherol 147, 222, 320 α-tomatine 151, 152, 155, 156 Abelmoschus manihot 248 Acacia auriculiformis 69 berlandieri 253 cambagei 252 colei 251, 252 colei var. colei 251 colei var. ileocarpa 251 confusa 254 crassa 252 cunninghamii 250, 251 delibrata 250 georginae 252, 254 holosericea 250, 253 nilotica 78, 231 penninervis 249 richii 294 rigidula 253 salicina 252 sparsiflora 252 Acacia Cedar 260, 261 Acanthophis antarcticus 80 Acerola 162, 221 acetogenin 385, 404, 405 acetylcholine 48, 133, 155, 216
Ackee 243, 244 Acremonium strictum 30 Acronychia acidula 110 Acrostichum aureum 346 speciosum 369 Actinopteris dichotoma 328 Adenia digitata 305 volkensii 305 Adiantum aethiopicum 328 capillus-veneris 327, 348 incisum 323 pedatum var. aleuticum 328 Aedes aegypti 216, 265, 286 African Dream Bean 74 African Honeybush 212, 227 Aiea Morning Glory 121 albicanol 347 Albizia adianthifolia 263 adinocephala 264 amara 259, 262, 264, 265 anthelmintica 260, 261, 263, 264 basaltica 258 chinensis 258, 262, 264 coriaria 264 falcataria 260, 263 fulva 263 hendersonii 258 julibrissin 259, 263 lebbeck 6, 259, 260, 261, 262, 263, 264 lophantha 258, 259 procera 261, 262 saman 258
saponaria 258, 259 sutherlandii 258 toona 260 vaillantii 259 versicolor 264 Alectura lathami 171, 248 Allium cepa 302 sativa 302 allo-ocimene 355 Almond Bark 413 Alocasia brisbanensis 50, 171, 172 crassifolia 195 cucullata 193, 195 indica 176, 195, 196 longiloba 194 macrorrhiza 16, 172 montana 189 Alphitonia excelsa 245, 246 ferruginea 246 oblata 245 petriei 246, 247 ponderosa 247 whitei 247 zizyphoides 246, 247 Alstonia constricta 237 Amaranth 186, 322 Amaranthus oleraceus 322 spinosus 96 amentoflavone 363 American Nightshade 136 aminophylline 270 Ammannia baccifera 239 Amoora rohituka 211 Amorphophallus albus 180 bulbifer 180 campanulatus 177, 461
178, 179, 184 galbra 177 gigantiflorus 178 konjac 65, 178, 179, 180 paeoniifolius 176 prainii 178 riveri 178 titanum 179 variabilis 178 Ampellocissus acetosa 79, 80 Ampelodesma tenax 135 amygdalin 412, 414, 415, 417 anabasine 252 Anacardium 200, 201, 202, 203, 204, 205, 206, 211, 215, 216, 217, 219, 220, 221, 239 humile 217, 220, 221 spondias 206 anacardol 216 Ananbaena circinalis 252, 399 cylindrica 396 flos-aquae 399 oscillarioides 396 Anaphe venata 318 anatoxin-a 399 Andrographis paniculata 271 Anemarrhena asphodeloides 212, 231 Anemia phyllitidis 335 Angiopteris evecta 314, 330, 348 Angular Pea 409 Anise Myrtle 110 Annona muricata 404 anthrax 304, 307, 308 Anthraxon lancifolius 134
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
Antiaris toxicaria 26, 178, 249 Aponogeton vanbruggenii 81 Apple 24, 136, 139, 140, 142, 162, 166, 236, 239, 273, 404, 413 Apricot 413, 414, 415, 417 arabinosa 382 Araucaria bidwillii 109 Archidendron grandiflorum 258 ramiflorum 258 vaillantii 259 Archirhodomyrtus beckleri 31 Argyreia 105, 123, 125, 126 nervosa 125, 126 Arisaema amurense 187 Arjuna 211 armarogentin 230 armentoflavone 347 aromadendrene 38 Arothron hispidus 403 Arrowroot Bermuda 65 Chinese 65 East Indian 65 Portland 65 Tahiti 65 Arsenic Plant 107 Arthropodium milleflorum 81 Artocarpus altilis 60, 109 Arum Lily 168 Arum maculatum 65, 176, 183 Ascaris lumbricoide 264 Asimina 404, 405 longifolia 404 triloba 404, 405 Asparagus racemosus 116 Aspergillus flavus 128, 179 aspidin 347 Aspidium athamaniticum 345 falcatum 345 spinulosum 344 Asplenium
adiantum-nigrum 327, 346 australasicum 348 filix-femina 344 furcatum 346 nidus 328, 347, 348 ruta-muraria 327, 346 Atala butterfly 356 Atropa belladonna 104, 105 Aubergine 136, 157, 158 Aulacaspis yasumatsui 391 Australian Marking Nut 109, 205 Australian Swamp Rat 412 australine 105 Avena sativa 135 Averrhoa bilimbi 178 Avicennia tomentosa 73 Azolla filiculoides 396 pinnata 322 azoxyglycosides 374, 393, 401 B β-carotene 53, 97, 98, 144, 145, 146, 147, 148, 162, 222, 226, 320, 364 β-caryophyllene 38 β-cryptoxanthin 144, 147, 148 β-glucosidase 417 β-myrcene 355 β-pinene 38 β-sitosterol 162, 165, 197, 222, 389, 397 β-thalassemia 231 Babesia 28 canis 28 duncani 28 gibsonii 28 microti 28 Baby Wood-Rose 125 Bacillus 37, 39, 75, 78, 83, 128, 163, 182, 188, 271, 283, 307, 311, 321, 324, 340 anthracis 307 cereus 37, 128, 163 mycoides 39
subtilis 37 Backhousia citriodora 110 Bacopa monniera 322 ‘Bag Shelter’ Moth 51 bagasse 214 BAPN 409 Barbados Cherry 162 barringtogenols 270 Barringtonia acutangula 265, 267, 268, 271, 272 asiatica 14, 266, 267, 271, 272 calyptrata 265 edulis 267 procera 267 racemosa 265, 270, 271, 272, 273 speciosa 266 Bat Plant 5, 67, 69, 70, 72 Beach Barringtonia 14, 266, 267, 271, 272 Beach Vine 106 Bean African Dream 74 Broad 408, 409, 410 Calabar 35 Horse 410 Jack 18, 20 Mackenzie 18 Mangrove 18, 20 Matchbox 72, 73, 76, 78, 282 Ordeal 12 Splinter 76 Beefheart Tomato 144 Beetroot 185 Belladonna 104 benzoic acid 225, 231 beriberi 318 Berlandier Acacia 253 Bermuda Arrowroot 65 Bermuda Grass 322 Beta vulgaris 185, 186 vulgaris var. cicla 185, 186 Betula 54 bilobetin 363 Bindweed 93, 104, 122 Biomphlaria glabratus 156
Bitter Almond 413, 414, 415, 417 Bitter Black Vetch 409 Bitterbark 237 Black Lily 69, 71, 374 Black Musli 82, 83 Black Pea 409 Black Sally Wattle 252 Black Spleenwort 327 Black Wattle 248, 252 Blackbean 16, 60, 61, 62, 63, 64, 105, 109 Blackwood 53, 56, 57, 248, 249 Blechnum cartilagineum 337 eberneum 337 indicum 337 milnei 338 orientale 337, 346 Blighia sapida 243 unijugata 244 Blind Disease 40 Blind Grass 40 Blind-your-eye Mangrove 16, 22, 23, 24, 25, 29, 197 Bloodroot 107, 108 Blue Flax Lily 40 Blue Grass Lily 81 Blue Perennial Pea 409 Blue Potato Vine 142 Blue Taro 188 BMAA 354, 363, 388, 389, 390, 391, 394, 395, 396, 397, 398, 400, 405 BOAA 405, 406, 407, 408 Bombax ceiba 228 Bombyx mori 319 Bopusia scabra 290 Boswellia serrata 212 Bowenia 6, 350, 351, 353, 355, 360, 361, 362, 364, 393, 394 eocenia 361 papillosa 361 serrulata 361, 362, 394 spectabilis 355, 360, 361, 394 Brachychiton gregorii
INDEX
110 Brassica oleracea 322 Breadfruit 60, 109 Bridelia ferruginea 286 Broad Bean 408, 409, 410 Broad Shield Fern 333 Brown Rat 412 Brush-tailed Possum 256 BSSG 389, 397 buggera-buggera 276 Bulrush 81 Bungwall Fern 336, 337 Bunya Pine nuts 109 Burdekin Plum 110 Burrawang 10, 352, 354, 357, 358, 367, 368, 376, 377, 378, 387 Bush Banana 110 Bush Bean 110 Bush Mango 273 Bush Melon 110 Bush Morning Glory 121 Bush Onion 81 Bush Orange 110 Bush Raisin 138 Bush Rat 256 Bush Sultana 138 Bush Tomato 110, 136, 137 Byfield Fern 362 C Cabbage 322, 370 Caesalpinia sappan 39 Caesia vittata 81 caffeic acid 100, 126, 145, 154, 325 caffeoylquinic acid 99, 100 Caju 217, 221 Calabar Bean 35 Caladium seguinum 191 Calamondin 51 California False Hellebore 152 Calla Lily 168 Calliandra pulcherrima 242 Callicarpa candicans 239 callicarpone 239 Callitris columellaris
336 Calophyllum inophyllum 239 Calystegia affinis 104 marginata 104 sepium 104, 105, 122 silvatica 104 Camellia sinensis 238 canatoxin 21 Canavalia 17, 18, 19, 20, 21, 58, 176 ensiformis 19, 20, 21, 176 gladiata 19, 21 maritima 19 obtusifolia 18 rosea 17, 18, 20 sericea 18 Canna achiras 65 edulis 65 Cape Gooseberry 136, 159, 160, 164, 165 Capparis mitchellii 110 spinosa 110 capsanthin 148 Capsicum annuum 148 annuum var. 148 angulosum annuum var. grossum 148 chinense 149 frutescens 149 pubescens 149 capsorubin 148 cardanol 203, 206, 212, 213, 214, 216, 220, 222, 223 cardol 203, 213, 216, 217, 222, 223 Carica papaya 162, 404 Carissa lanceolata 110 Carrion flower 253 Caryophyllene 37 Caryophyllus aromaticus 189 Cassava 65, 184, 248, 370, 386, 401, 411, 412, 414 cassowary 15 Cassowary Pine 265
463
castanospermine 63, 105 Castanospermum 16, 61, 62, 63, 109, 375 australe 61 Castor oil plant 274, 308 Casuarius casuarius johnsonii 15 Catakidozamia hopei 364 catechin 154, 221, 225, 231 Catsear 84 Cayenne Pepper 149 CBA 308 Cedar Bay Cherry 110 Celery-leaved Buttercup 198 Celosia argentea 48, 156 Ceratozamia mexicana 394 Cetraria islandica 347 Champion Bay Poison 256 Cheeky Yam 81, 109 Cheilanthes albomarginata 324, 325 anceps 325 chrysophylla 324 contracta 325 covillei 324 dalhousiae 324 farinosa 323, 325 glauca 325 hirta 324 kaulfussi 324 lasiophylla 323 pruinata 324 sieberi 322 tenuifolia 322, 324, 328 tomentosa 324 viridis 324 wootoni 324 chelidonic acid 109 Cherry Beech 237, 238 Cherry Laurel 413, 414 Cherry, Wild Black 414 Chickling Pea 405 Chickling Vetch 406 Chicory 84 Chilean Perennial Pea 409 Chillagoe Horse Poison
408 Chinese Arrowroot 65 Chinese Lantern 136, 159, 163 Chlorella vulgaris 197 Chloris barbata 322 Chokecherry 414 Chondrodendron tomentosum 12 Christella dentata 323 Chrysanthemum coronarium 97 morifolium 99 chrysophanic acid 43 Cichorium intybus 84 ciguatera 403 ciguatoxin 403 Cimicifuga 54 Cinnamon Fern 334 Cissus adnata 79 Citrus australasica 110 glauca 110 mitis 51 sinensis 162 Claviceps africana 135 fusiformis 134 purpurea 129, 133, 134, 135 Clematis vitalba 198 Clostridium botulinum 153, 182, 307 perfringens 182 tetani 210 CNSL 213, 214, 216, 220 Coast Myall 252 Coastal Morning Glory 120 Cochlospermum gillivraei 415 Cockscomb 156 Cocky Apple 273 Cocoyam 188, 189 Cocoyams 65, 188, 192 Colocasia antiquorum 170, 193, 195, 197 antiquorum var. esculenta 197 esculenta 65, 109, 169, 170, 171, 176,
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
181, 183, 184, 188, 195, 196, 197 esculenta fonatinesii 171 macrorhiza 50 Commelina africana 291 Commiphora mukul 211, 212 Common Morning Glory 116, 119, 121 concanavalin A 21, 176 Confederate Spiderwort 334 coniine 11, 177 Conium maculatum 11 Conkerberry 110 convicine 410 Convolvulus arvensis 96 nervosus 5, 126 nil 112, 119 scammonia 101, 114, 115 turpethum 115, 117, 120 Coolibah 237 Coontie 370 Copaifera 78 Cordyline fruticosa 97 Corn Buttercup 198 Corpse Flower 179 Creeping Buttercup 198 Cretan Brake 322, 323 Crimean Snowdrop 253 Crimson Morning Glory 124 Crotalaria aridicola 408 crispata 407 juncea 114 medicaginea 407 mitchellii 407 novae-hollandiae subsp. novaehollandiae 407 pallida 407 ramosissima 407 retusa var. retusa 407 spectabilis 407 Croton tiglium 300 Crowfoot 198 Cryptocarya bancrofti 64 Cubè 281
Cuckoo Pint 183 Cucumber tree 178 Cucumis melo 110 Cunjevoi 16, 50, 168, 169, 170, 171, 172, 182, 183, 189, 190, 191, 192, 193, 194, 195 Cupania pseudorhus 242 curare 12, 190 curcin 300 Curculigo crassifolia 83 orchioides 82, 83 curculigoside 83 Curcuma angustifolia 65 longa 65, 302 Currawang 252 cuscohygrine 141 Cutnut 267 cyanobacteria 251, 252, 385, 394, 395, 396, 398, 399, 400, 401, 402 Cyathea cooperi 314, 330 Cycadothrips albrechti 355 chadwicki 355 Cycas 6, 9, 17, 61, 91, 349, 351, 352, 353, 355, 357, 361, 365, 366, 367, 369, 370, 372, 374, 375, 376, 378, 379, 380, 381, 382, 383, 384, 386, 387, 388, 389, 390, 391, 392, 393, 394, 395 angulata 352 armstrongii 352, 353 cairnsiana 366, 383 calcicola 352, 353 canalis 352, 353 canalis subsp. canalis 353 circinalis 351, 378, 379, 380, 381, 386, 387, 388, 391, 394, 395 media 17, 349, 351, 352, 355, 357, 365, 367, 369, 370, 374,
375, 376, 394 media subsp. banksii 376 megacarpa 366 micronesica 386, 390, 391, 394, 395 neocaledonica 380 ophiolitica 352, 366 platyphylla 366 revoluta 351, 375, 378, 381, 382, 383, 386, 388, 391, 394, 395 rumphii 353, 378, 379, 380, 381, 382, 383, 391, 392 rumphii subsp. normanbyana 353 thouarsii 353 tuckeri 352 cycasin 354, 356, 357, 363, 374, 379, 383, 386, 388, 389, 390, 393, 394, 397 Cyclopia genistioides 212 subternata 227 Cyclosorus interruptus 337 Cylindrospermopsis raciborskii 396, 398, 399 Cynodon dactylon 322 Cyperus bulbosus 81 macrostachyos 81 rotundus 322 Cyrtosperma chamissonis 184 D daidzein 287 Damson 237, 415 Dandelion 84 Daphne genkwa 29, 30 Datura inoxia 102 metel 208 Davallia tenuifolia 327 Davidsonia jerseyana 110 Daylily 41 Death Adder 80 deguelin 280, 281, 282, 283, 286
Dendrocnide 5, 44, 45, 46, 47, 48, 50, 53, 54, 55, 56, 57 corallodesme 44, 47 cordata 44 cordifolia 44 decumana 53, 56 excelsa 44, 46, 47, 50, 54 moroides 44, 45, 46, 47 peltata 44 peltata var. peltata 44 photinophylla 44, 46 sinuata 44, 48, 57 Denhamia obscura 258 Dennstaedtia punctiloba 334 dennstoside A 323 deoxoglycyrrhetol 297 dephinidin 113 Derris elegans 279 elliptica 276, 277, 278, 282 forsteriana 275 involuta 277 koolgibberah 276 purpurea var. purpurea 291 scandens 282, 283 trifoliata 275, 276, 277, 279, 281, 283 uliginosa 275, 276, 283 Derris Preparata 277 desaspidin 347 Desert Fringed Lily 80 Desert Kurrajong 110 Desert Lime 110 Desert Yam 103 Devil Nettle 48 D-glucose 333 diaminobutyric acid 400 Dianella 40, 41, 42, 43, 81 caerulea 40, 41, 42 callicarpa 43 ensifolia 42, 43 laevis 40, 81 longifolia 40 longifolia var. grandis 43 nemorosa 42
INDEX
revoluta 40, 43 revoluta var. revoluta 43 sandwicensis 43 tasmanica 42 dianellidin 43 Dianthus crenatus 291 Dichapetalum cymosum 256 Dicksonia antarctica 335 Dieffenbachia picta 189 seguine 176, 189, 190, 191 dieldrin 145, 401 Dioon edule 357, 383, 394 spinulosum 359, 383 diosbulbins 88 Dioscorea 5, 16, 61, 65, 68, 69, 76, 79, 81, 84, 85, 86, 87, 88, 89, 90, 91, 92, 93, 96, 109, 176, 177, 181, 182, 184, 197, 259, 374 alata 5, 86, 87, 88, 91, 92, 93, 96, 197 bulbifera 69, 76, 79, 86, 87, 88, 89, 109, 177 bulbifera var. bulbifera 89 dumetorum 68 esculenta 68, 96, 181, 182, 184 pentaphylla 87 sansibarensis 90 sativa var. rotunda 90 transversa 79, 85, 86, 87 dioscorin 93 Diospyros mespiliformis 239 Diplazium esculentum 323 Diplococcus pneumoniae 39 divicine 410 Doryanthes excelsa 94 Drynaria quercifolia 346 Dryopteris athamantica 345 atrata 342
carthusiana 346 crassirhizoma 346 cycadina 342 dilatata 328, 345 filix-mas 315, 322, 326, 342, 343, 345, 347 hasseltii 342 inequalis 345 juxtaposita 322, 323 marginalis 343 parallelogramma 345, 346 sparsa 342 Duboisia hopwoodii 251, 252 Duckweed 321, 322 Dumbcane 168, 176, 189, 190, 191 E East Indian Arrowroot 65 Eggplant 136, 152, 153, 157, 158 Elecampane 84 Eleocharis acuta 81 nuda 81 sphacelata 81 Elephant Creeper 5, 126 Elephant-foot Yam 176, 178 elephantiasis 28, 75, 126 Elephantorrhiza goetzei 302 ellagic acid 30, 99, 226, 270 Emblica officinalis 211 Encephalartos 350, 351, 357, 364, 373, 375, 376, 382, 383, 393, 394 arenarius 394 ferox 383 hildebrandtii 373 longifolius 373 miquelii 375 spiralis 376 transvenosus 373 trispinosus 394 villosus 394 Entada abyssinica 75, 76, 78
465
africana 76, 77, 78, 264, 282 phaseoloides 72, 73, 74, 75, 76, 78 polyphylla 76 purseatha 77 rheedei 72, 74 scandens 74 spicata 75, 76 Entamoeba histolytica 225, 261, 268, 312 Enterococcus 30, 37, 271, 311 faecalis 37, 271, 311 epicatechin 154, 225, 231, 261 ergocornin 132 ergocriptine 132, 133 ergocristine 118, 132, 133 ergometrine 125, 132, 133 ergonovine 133 Ergot 5, 123, 124, 129, 130, 131, 132, 133, 134, 135 ergotismus convulsivus 130 gangraenosus 129 eriocitrin 227 Ervatamia dichotoma 226 Ethiopian Eggplant 158 etiopine 192 Eucalyptus 10, 51, 80, 139, 237, 336, 358 corymbosa 336 loxophleba 80 maculata 358 microtheca 10, 237 sieberi 336 sieberiana 336 Eugenia reinwardtiana 110 Eumaeus atala 356 Eurema hecabe mandarina 335 European Black Nightshade 136 European Mountain Pea 409 Everlasting Pea 409 Excoecaria 16, 22, 23, 24, 25, 26, 27, 28, 29,
30, 31 acerifolia 29, 30 agallocha 26 agallocha var. agallocha 23 agallocha var. ovalis 23 cochinchinensis 26, 28, 29 dallachyana 27 indica 25 macrophylla 25 oppositifolia 25 parvifolia 25, 29, 30, 31 venenifera 25 Exogonium purga 114 F Falcataria moluccana 260 False Sago Palm 379, 381, 386 Faradaya amicorum 248 parviflora 248 splendida 248 Fenugreek 181 Fever Nettle 48 filicin 342, 343 filmarone 346 Finger Cherry 5, 16, 31, 33, 34, 35, 36, 39 Finger Lime 110 Fish Poison Tree 6, 14, 271 Five-finger Fern 328 Five-leaf Yam 87 Flannel Bush 139 Flax Lily 40, 42, 81 Floating Primrose Willow 322 Flowering Bloodroot 107 Forest Nightshade 141 Fragaria vesca 162 Freshwater Mangrove 267, 268 fucose 382 fuju 403 Fusarium solani 102 G Galactia 294
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galactose 181, 218, 382 gamma-carotene 144 Garcinia cherryi 238 mangostana 229, 238 Garden Geranium 216 Garland Chrysanthemum 97 Gastrolobium bilobum 256 gelonin 305 Gelonium multiflorum 305 genistein 282, 283, 286, 287, 288 Gentiana lutea 230 Georgina Gidyea 252, 254 Giant Bindweed 104 Giant Fern 314 Giant Stinging Tree 44, 47, 50, 53, 54 Giant Sweet Potato 99 Giant Taro 168, 184 Giardia intestinalis 225 Gidgee 252, 254, 255, 274, 295 Gidgee Gidgee 274, 295 Gidyea 252, 254 ginkgetin 363 Ginkgo biloba 206, 363 ginsenosides 242 globulol 38 Gloeosporium periculosum 34, 36 Glycine max 185, 242, 287 Glycyrrhiza glabra 211, 242, 296, 297 glycyrrhizin 296, 297, 298 gokhru 116 Goldenberry 161, 162 Goobang 248, 249 Grass Pea 405, 406 Grass Yam 82 Grass-leaved Convolvulus 103 Greater Yam 87, 88, 91, 92, 93, 96 Green Kangaroo Apple 140 Grey Kangaroo 256 Grey Rhodomyrtus 32
Guaiacum officinale 284, 294 Guava 31, 37, 39, 232 Gum-guggal 211 Gunnera kauaiensis 396 petaloidea 396 Gunyang 140 Gutta Percha 30 Gyamkawa 281, 282 Gymea Lily 94 Gympie Bush 44 gympie gympie 52 H haemocorin 107, 108, 109 Haemodorum coccineum 107, 108 corymbosum 108 laxum 107 spicatum 107, 108 Haemonchus contortus 264 Hairy Yam 88 Harpagophytum 54 Hay-scented Fern 334 Heart-leaf Poison 256 Heavenly Blue Morning Glory 124 Hedera helix 204, 205 Hedyotis hispida 324 Helianthus tuberosus 84, 85 Helicobacter pylori 220, 272, 282, 293, 331 Hell Oil 300 hemerocallin 41 Hemerocallis fulva 41 Hemidesmus indicus 211 Hemlock 11 Herpes genitalis 154 simplex 154 zoster 154 hesperidin 227 Hibiscus subdantta 110 Hippomane mancinella 23, 24 histamine 46, 48, 88, 133 Honeysuckle 301 hordenine 252, 253 Hordeum vulgare 253
Horse Bean 410 Hura crepitans 239 huratoxin 239 hyaluronic acid 215 hydrocyanic acid 412 Hygrophila schulli 322 Hyoscyamus niger 165 Hypericum 227 Hypocheris radicata 84 hypoglycin B 244 hypoloside 323 I Icelandic Moss 347 ichthyotereol 239 Ichthyothere terminalis 239 Illawarra Plum 110 illudane 332 illudin 333 indanones 333 Indian Beech 286, 287 Indian Gooseberry 165 Indian Guggulu 211 Indian Liquorice 295 Indian Nightshade 139 inophyllolide 239 Interrupted Fern 334 Inula helenium 84 ipomeamarone 102 Ipomoea 5, 65, 81, 84, 95, 96, 97, 98, 99, 100, 101, 102, 103, 104, 105, 106, 111, 112, 113, 114, 115, 116, 117, 118, 119, 120, 121, 122, 124, 125, 184, 197 aegyptia 122 alba 102 angustifolia 103 aquatica 96, 99, 100, 101, 111 batatas 65, 95, 97, 98, 99, 184, 197 cairica 116, 118 calobra 106 costata 103 digitata 99, 111, 116, 117, 118 eriocarpa 100 fistulosa 111 graminea 103 hederacea 111, 112,
114 indica 95, 122 macrantha 111 mauritiana 99, 102, 111, 117, 118 muricata 114 nil 99, 112, 113, 119 orizabensis 113, 114 pes-caprae 106 pes-tigridis 121 pes-tigridis var. longibracteata 121 polpha 81, 103, 104, 105 polpha subsp. latzii 103 polpha subsp. weirana 105 purga 113, 114, 116, 120 purpurea 116, 119 quamoclit 121 sinuata 122 tricolor 124 turpethum 115, 116, 117, 120 Ironwood 31, 32 isoginkgetin 363 isomangiferin 225, 227, 228 isouramil 410 Ivy 119, 121, 159, 197, 198, 204, 205, 208, 209 Ivy-leaved Ground Cherry 159 Ivy-leaved Morning Glory 121 J Jack Bean 18, 20 Jack O’Lantern Mushroom 333 Jagera pseudorhus 242, 243 Jalapa 108, 113 Japanese Fern Palm 381, 382, 388 Jatropha curcas 165, 300, 312, 313 manihot 410 jatrophin 300 Jequirity 295, 296, 297
INDEX
Jerusalem Artichoke 84, 85 Jerusalem Cherry 136 Juglans mandshurica 239 juglone 239 Jussiaea repens 322 Justicia hayatai var. decumbens 239 K kaempferol 29, 127, 147, 225, 271, 347 Kakadu Plum 110 Kaladana 112, 113, 114 Kang Kong 101 Kangaroo Apple 136, 140 karanjin 280, 281 Karenia brevis 397, 402 Kesari 405, 406 King Fern 314 Klebsiella 128, 271, 311 Kodo Millet 322 Kolavenol 78 Konjac 65, 178, 179, 180, 181, 182 Koorti 370 Kudzu 288 Kulyu 106 Kunzea pomifera 110 L Lace Lizard 193 Lachnanthes caroliniana 108 lactagogue 118, 127, 131, 312, 313 Lactococcus lactis 196 Lacy Tree Fern 314 Laetrile 417 Laportea crenulata 47, 56 decumana 53, 56 gigas 44 pustulosa 48 stimulans 48, 57 Large Annual Buttercup 198 Lastrea athamantica 345 lathyrism 405, 408, 411 Lathyrus angulatus 409
cicera 405, 406 clymenum 405 grandiflorus 409 latifolius 409 montanus 409 niger 409 ochus 405 odoratus 408, 409 pubescens 409 sativus 405, 406, 409 sphaericus 409 sylvestris 280, 409 tingitanus 409 Leishmania donovani 241 Lemon Aspen 110 Lemon Myrtle 110 Lepidozamia 6, 350, 351, 353, 354, 355, 356, 360, 364, 365, 380, 394 hopei 364, 365, 394 peroffskyana 354, 355, 356, 365 Lesser Celandine 198 levodopa 401, 404 Lily Arum 168 Black 69, 71, 374 Blue Flax 40 Blue Grass 81 Calla 168 Desert Fringed 80 Flax 40, 42, 81 Gymea 94 Peace 8, 168 Vanilla 81 limonene 37 linalool 357 linamarin 411, 414 lipase 88, 308, 310 Liquorice 163, 211, 242, 295, 296, 297, 298, 301 Littlebell 121 Lonchocarpus cyanescens 280, 283 floribundus 280 latifolius 280 montanus 281, 283 urucu 280, 283 utilis 280, 283 Long Yam 79, 80, 81, 86, 87
467
Long-leaf Pawpaw 404 Long-leaved Ground Cherry 159 Lonicera japonica 301 Lophophora williamsii 253, 254 lotaustralin 411, 414 Lotus 66, 67 Lucea Yam 182 Lucky Grass 97 lupeol 31, 261, 270, 294 lycopene 144, 145, 146, 147, 155, 272, 364 Lycopersicon esculentum 136, 152, 156 esculentum var. cerasiforme 156 pimpinellifolium 155 Lycopodium funiforme 328 laxum 328 phlegmaria 328 selago 345 Lymnaea cubensis 156 M Macadamia integrifolia 109 MacDonnell Ranges Cycad 352 Mackenzie Bean 18 Macropus fuliginosus 256 Macrozamia 10, 350, 351, 352, 353, 354, 355, 356, 357, 358, 359, 361, 364, 367, 368, 371, 375, 376, 377, 380, 381, 382, 384, 386, 387, 393, 394, 406, 407, 410, 411 communis 352, 355, 358, 368 fraseri 384 lomandroides 352 lucida 355, 358 macdonnellii 352, 355 machinii 355 montana 358 moorei 352, 358, 359, 406, 407 pauli-guilielmi 352,
353 riedlei 371, 375 spiralis 10, 357, 358, 361, 368, 376, 377, 386, 387 macrozamin 354, 357, 363, 386, 393, 394 Maidenhair 206, 324, 326, 327, 328, 348 Maidenhair Fern 324, 327, 328 maitotoxin 403 Malay Jewel Vine 283 Male Fern 315, 322, 326, 340, 342, 343, 344, 345 Mallotus apelta 286 Malpighia glabra 162 Malus domestica 162 MAM 389 Mammea africana 239 Mammy Apple 239 Manchineel Tree 23, 24 maneb 401 Mangifera altissima 226 caesia 223 indica 6, 205, 223, 224 longipetiolata 224 minor 226 sylvatica 224 mangiferone 224 Mango Tree 6, 212, 223, 232 Mangosteen 229, 238 Mangrove Milky 16, 22, 23, 24, 26, 27, 28, 30, 31 Ovate-leafed Milky 23 Mangrove Bean 18, 20 Manihot esculenta 65, 411, 414 utilissima 412 mannose 176, 181, 218, 382 Mapoon 257 Maranta allouya 65 arundinacea 65 nobilis 65 Mariana Flying Fox 390 Marsilea angustifolia 316 drummondii 313, 315
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
minuta 316, 320, 321 quadrifida 321 quadrifolia 321 villosa 322 marsilin 320 marsiline 320 Mastocarpus stellatus 253 Matchbox Bean 72, 73, 76, 78, 282 Matteuccia orientalis 334 struthiopteris 334, 335, 346 Meadow Buttercup 198 MeDAP 389 melanin 197, 388 Melanotranes internatus 356 Melilot 257 Melilotus indica 257 Merremia dissecta 122 peltata 119, 123 mescaline 253 methylazoxymethanol 389 methylepigallocatechin 232 methylrhamnose 382 methylsalicylate 357 microcystin 398, 400, 401 Microcystis aeruginosa 252, 399 Microseris lanceolata 84, 85 Microzamia spiralis 368 Mile-a-Minute 125 Milky Mangrove 16, 22, 23, 24, 26, 27, 28, 30, 31 Millettia australis 284 dasyphylla 284 dielsiana 285 dura 286 eriocalyx 285 extensa 285 griffoniana 286 hemsleyana 284 leucantha 286 megasperma 2, 284 nitida 285
pachycarpa 284, 286 pendula 286 pinnata 280, 286 reticulata 285, 286 sericea 284 taiwaniana 286 thonningii 285 usaramensis subsp. usaramensis 285 zechiana 285 Mimosa pigra 78 Miscanthus sinensis 415 Mistletoe 305 Modecca digitata 305 modeccin 305 Moniezia 175, 264 Monkey Rose 125 Monochoria hastata 322 vaginalis 322 Monstera deliciosa 168 Moonflower 102, 120 Moreton Bay Chestnut 61 Morinda reticulata 257 morphine 21, 227 Mother Shield Fern 333 Mouse Guava 31, 37, 39 MPTP 401 MRSA 37, 217, 283, 346 Mucua pruriens 116 Mulga Fern 322, 324 Mundulea sericea 281, 282 Muntries 110 Murnong 84 Mycobacterium phlei 37, 380 smegmatis 217, 271 tuberculosis 128, 194, 293 Myoporum 102, 255 myosmine 252 Myrtus trineura 32 N Narcissus pseudonarcissus 176 Nardoo 313, 315, 316, 317, 319, 322 Nardoo Fern 315, 316, 317 Native Cashew 16, 204 Native Grape 79, 80
Native Mint 110 Native Raspberry 110 Native Sweet Potato 103, 104, 109 Native Wisteria 284 Nauclea latifolia 286 Nelumbo nucifera 65, 66 nerirutin 227 Neptunia amplexicaulis 257 Nicandra physaloides 166 nicotine 152, 153, 252 Nigella sativa 211 NMDA 389 Nocardia asteroides 401 Nodding Blue Lily 40 Nodularia spumigena 252, 398 nodularin 400 nornicotine 252 North American Pawpaw Tree 404 Nostoc commune 396 flagelliforme 396 punctiforme 396 Nothofagus grandis 340 notoginsenosides 242 O Ocimum basilicum 114 sanctum 211 October Glory Vine 248 Oecophylla smaragdina 235 Ololiuqui 124 Omphalotus illudens 333 Onion Vine 117 onjisaponins 242 Onychium contiguum 323 Operculina aequisepala 117 riedeliana 117, 120 turpethum 115, 117, 120 Ophioglossum pendulum 328 Ordeal Bean 12 Orizaba 114 osajin 283 Osmunda
cinnamonea 334 claytoniana 334 japonica 334, 335, 346, 347 regalis 334, 335 osteolathryism 408 Ostrich Fern 334, 335 Oswego Arrowroot 65 Ovate-leafed Milky Mangrove 23 Oxalabacter formigenes 185 Oxylobium ellipticum 255, 256 Ozoroa insignis 302 P Pacific Chorus Frog 397 Pacific Mosquito Fern 396 Palm-leaved Tacca 71 Panax notoginseng 242 Pandanus spiralis 9 paracetamol 270 Paradicsom paprika 148 paraquat 401 Paraserianthes toona 260, 261 Passiflora foetida 236 Pawpaw 162, 404 Peace Lily 8, 168 Peach 413, 414, 415, 416, 417 Peganum harmala 114 Pelargonium x hortorum 216 Pellaea atropurpurea 346 Pencil Yam 81 Pentarhizidium orientale 334 pentobarbitone 21, 158 Peruvian Torch Cactus 253 Petford Cycad 366 Peyote 253 Pharbitis nil 112, 119 phloroglucinols 347 physalin 160, 161, 162, 165 Physalis alkekengi 136, 158, 159, 160, 161, 162, 163
INDEX
angulata 158, 159, 160, 161, 162, 163, 165 crassifolia var. versicolor 159 hederifolia 159 ixocarpa 159, 164 micrantha 159 minima 159, 160, 162, 163, 164, 165, 166 peruviana 159, 160, 161, 162, 164, 165, 166 philadelphica 159, 166 pubescens 159, 162, 164 Physic Nut 300 Physostigma venenosum 12, 35 physostigmine 12, 24, 35 phytohaemagglutinin 21 Phytolacca decandra 305 Pigweed 81, 319 Pilidostigma papuanum 31 Pilinut 267 pilocarpine 12 Pilocarpus jaborand 12 Pink Ash 246 Pink Laceflower 258 Piscicide 12 Pistachio Tree 205, 206 Pistacia vera 205, 206 Pistia stratiotes 321, 322 Pisum sativum 409 Pithecellobium grandiflorum 258 pithecelobine 259 pithecolobine 259 Planchonia careya 273 Plasmodium falciparum 264, 272, 285 Platycephalus 28 platycodins 242 Platycodon grandiflorum 242 platycoside E 242 Platysace deflexa 107 Pleiogynium timorense 110 Plum 110, 413, 414, 415 Plumbago indica 211
zeylanica 211 plygalasaponins 242 Podocarpus elatus 110 Poi 86, 196 Poison Elder 209 Poison Rope 274, 276 Pokeweed 305 Polygala tenuifolia 242 polygodial 238 Polygonum hydropiper 238 orientale 238 Polypodium aureum 347 glycyrrhiza 347 hastatum 327 polypodioides 345 polypodoside A 347 Polystichum australiens 333 fragil 333 munitum 328 omeiense 333 proliferum 333 pungens 332 richardii 332 squarrosum 323, 332 whiteleggei 333 Polysticium formosanum 333 Pongamia pinnata 280, 281, 286 pongamol 280, 281, 282, 283 Portland Arrowroot 65 portulac 319 Portulaca oleracea 81, 319 pilosa 320 potassium cyanide 412, 413 Potato Bush 139 Potato Yam 89, 96 Prasyptera mastersi 49 Precatory Bean 6, 274, 275, 295, 296, 299, 300, 301, 302, 303, 304, 306 Prickly-toothed Shield Fern 344 Prorodes mimica 49 prosapogenin 78 Prostanthera incisa 110 protanemonin 198
469
Proteus vulgaris 128, 311 protoanemonin 199 prunasin 332, 335, 414, 415 prunin 415 Prunus amygdalus 413, 414 armeniaca 413, 414, 415 avium 413 brachystachya 413 campanulata 413 domestica 413 dulcis var. amara 413, 414 grisea var. grisea 413 laurocerasus 413, 414 melanocarpa 414 pensylvanica 414 persica 413, 414, 415 persica var. davidiana 415 serotina 414 turneriana 413 virginiana 159, 414 virginiana var. melanocarpa 414 prussic acid 417 Pseudacris regilla 397 Pseudomonas aeruginosa 83, 119, 174, 271, 311, 321, 324 exotoxin 305 pseudoalcaligenes 30 Psidium guajava 39, 232 Psychotria ipecacuanha 269 ptaquiloside 322, 323, 332, 333, 334, 338, 339 pteridin 339 Pteridium aquilinum 322, 325, 326, 329, 335, 338, 341, 346 aquilinum subsp. aquilinum 325 aquilinum subsp. caudatum 325 aquilinum subsp. decompositum 326 aquilinum var.
esculentum 329 esculentum 326 Pteris aquilina 326, 341 cretica 322, 323 excelsa 323 inequalis 340 vittata 335 Pterocarpus angolensis 302 diadelphus 275 Pteropus conspicillatus 393 mariannus 390, 392 tokudae 392 pterosin B 333, 334 pterosins 333, 334, 340 Pueraria lobata 287, 288 mirifica 288 montana var. lobata 288 tuberosa 288 pufferfish 403 pulcherrimasaponin 242 Puna yam 182 Purging Croton 300 Purging Nut 300 Purple Moonflower 102 Purslane 319, 320 Pygeum turnerianum 413 Q Quandong 110 Queensland Jam Plant 110 quercetin 127, 147, 162, 179, 225, 226, 293, 336 quillaic acid 240 Quillaja 240, 241, 242, 243, 245 saponaria 240 R Railway Creeper 116, 121 Ranunculus acris 198 bulbosus 199 flammula 199 repens 198 Rat
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
Australian Swamp 412 Brown 412 Rattus fuscipes 256 lutreolus 412 norvegicus 412 Red Almond 247 Red Ash 245, 246 Red Bell Pepper 148 Red Convolvulus 121 Red Nut Sedge 322 Red Siris 260 Red-legged Pademelon 49 Redroot 108 Reineckia carnea 97 Revwattsia fragile 333 rhamnose 218, 382 Rheedii 74 rheediinosides 78 Rhipidura leucophrys 367 Rhizoctonia solani 262 Rhizoma arisaematis 195 pinelliae 195 Rhodnius prolixus 161 rhodomyrtoxin 37 Rhodomyrtus 16, 31, 32, 33, 34, 35, 37, 38, 39 beckleri 31 canescens 31, 37 effusa 31, 32 macrocarpa 16, 31, 33, 34, 35 pervagata 31, 32 psidioides 31 recurva 31 sericea 31 tomentosa 31, 37, 39 trineura 31, 32 trineura subsp. capensis 38 Rhopalotria slossonae 357 Rhus verniciflua 210 Rhyncharrhena linearis 110 Ribbon Fern 328 Riberry 110 riboflavin 97 ricin 274, 299, 301, 302, 304, 305, 306, 307, 308, 311, 313
ricinine 308, 312 Ricinus communis 12, 274, 275, 299, 300, 305, 312, 410 Rivea corymbosa 123, 124 River Poison 256 Rock Fern 324 Rock Poison 256 Rosary Pea 295 Rosella 110, 147 rotenoid 294 rotenolone 280, 281 rotenone 77, 274, 277, 278, 279, 280, 281, 282, 283, 284, 285, 290, 313, 401, 405 Round Yam 69, 79, 86, 87, 88, 89, 90, 91 Round-leaf Yellow Yam 182 Royal Fern 334, 335 Rubus moluccanus 110 Rusty Rhodomyrtus 32 S Sacred Basil 211 Sadleria pallida 335 Salacia 227, 231, 232 chinensis 231 disepala 231 oblonga 231 reticulata 232 Salmonella typhimurium 155 Saltbush 81 Samanea saman 258, 259 San Pedro Cactus 253 Santalum acuminatum 110 Sapindus mukorossi 245 Saponaria officinalis 305 saporin 305 Sarcina lutea 228 saxitoxin 307, 399, 401, 402 Scammony 101, 112, 113, 114, 115 Scammony Resin 113 scandinone 283 scaritoxin 403 Scarlet Creeper 121
Schistosoma japonicum 78 scrofula 194 Scrub Nettle 53 sebacic acid 310 Selaginella sinensis 347 Semecarpus atra 203 australiensis 16, 200, 201, 202, 204, 210 australis 110 cassuvium 203, 207 cuneiformis 207 heterophylla 207 Semecarpus Lehyam 211 serotonin 48, 124, 133, 320 Shaggy Shield Fern 342 shatavari 116 Shigella 30, 56, 128, 163, 304, 321 dysenteriae 304 shikimic acid 335 Shining-leaved Stinging Tree 44 Shoo-fly Plant 166 Showy Rattlepod 407 Silk Cotton Tree 228 Silkworm 318, 319 Silky Jackbean 18 Silver Morning Glory 125, 126 Silvertop Ash 336 Siris Tree 260 Slender Wild Pea 409 Small White Morning Glory 121 Soap Bark 240 Soap-nut Tree 245 solamargine 154, 155, 156 solamine 141 solanidine 137 solanine 137, 142, 150, 151, 152, 154, 155 solanocapsidine 137 solanocapsine 137 Solanum 5, 15, 95, 104, 110, 136, 137, 138, 139, 140, 141, 142, 143, 149, 151, 152, 153, 154, 155, 156, 157, 158 aethiopicum 158
americanum 154 armatum 140 aviculare 136, 140 capsicoides 142 centrale 137 chippendalei 138, 139 citrinitum 155 coactiliferum 139 dimorphispinum 151 dulcamara 155 dunalianum 151 hystrix 139 incanum 155 insanum 157 lanciniatum 153 linnaeanum 142 melongena 136, 152, 157, 158 nigrum 136, 155 orbiculatum 139 phureja 149 prinophyllum 141 pseudocapsicum 136, 137 quadriloculatum 139, 140 seaforthianum 142 sisymbriifolium 141 sodomaeum 142, 155 tuberosum 5, 95, 104, 136, 154 vescum 140 solasodine 137, 141, 142, 152, 153 solasonine 142, 151, 152, 153, 154, 155, 156 solcaproine 141 Sorghum Ergot 135 Soursop 385, 404 Soybean 185, 287 Spatholobus suberectus 285 spathulenol 37, 38 Spectacled Flying Fox 393 sphaerobioside 283 Spike Rush 81 Spinacia oleracea 186 Spirodela polyrhiza 321 Spirostachys africana 25 Splinter Bean 76 Spondias mombin 206 Spotted Gum 358
INDEX
Spurred Vetch 410 St John’s Wort 227 Stangeria 350, 351, 362, 363, 364, 394 eriopus 362, 363 Stapelia gigantea 253 staphylococcal enterotoxin B 307 Staphylococcus 30, 37, 39, 56, 83, 101, 128, 154, 161, 163, 174, 182, 220, 228, 271, 283, 290, 303, 307, 311, 321, 324, 346, 380, 381 aureus 37, 39, 128, 154, 161, 163, 174, 182, 220, 271, 283, 307, 311, 321, 381 epidermidis 37 stephanotic acid 48 Stephanotis floribunda 48 Sterculia tomentosa 382 Sticky Nightshade 141 Stictocardia beraviensis 124 tiliifolia 125 stigmasterol 222, 270 Stinging Tree Giant 44, 47, 50, 53, 54 Shining-leaved 44 Strawberry 162, 232 Strawberry Guava 232 Streaked Rattlepod 407 Streptococcus 37, 39, 128, 161, 199, 217, 220, 232, 261, 311 gordonii 37 haemolyticus 39 mutans 37, 161, 217, 220 pneumoniae 37 pyogens 37, 311 salivarius 37 typhi 37 strychnine 12, 379 Strychnos 12, 211, 212, 249 nux vomica 211 potatorum 211 Stypandra glauca 40
imbricata 40 styphandrol 40 styphandrone 40, 43 swainsonine 105 Sweet Potato 65, 68, 95, 96, 97, 98, 99, 100, 101, 102, 103, 104, 106, 109, 118, 120 Swertia chirata 227, 231 Swiss Chard 185 Swiss-Cheese Plant 168 Sword Bean 19, 20, 21 Sword Fern 328 Syzygium anisatum 110 aromaticum 189 cuminii 231 forte subsp. potamophilum 236 luehmannii 110 T Tacca chantrieri 71, 72 hawaiiensis 69 integrifolia 71, 72 involucrata 67, 69 leontopetaloides 67, 69, 70, 81, 374 palmata 71 pinnatifida 65, 69 Taenia solium 346 Tahiti Arrowroot 65 Tangier Pea 409 Tapioca 68, 197, 248, 410, 411, 412 Tar Tree 16, 201, 202 Taraxum officinale 84 Taro 65, 96, 109, 167, 168, 169, 170, 171, 172, 180, 182, 183, 184, 186, 187, 188, 192, 193, 195, 196, 197 Tasmanian Pepperberry 110 Tasmannia lanceolata 110 Teara contraria 52 Temple Plant 322 tenuifolisaponins 242 Tephrosia aequilata 291 atroviolacea 289
471
bracteolata 289, 291 289 candida capensis 289, 291 densiflora 289, 291 diffusa 289, 291 filipes 292 kraussiana 291 linearis 289 lucida 291 macropoda 290, 291 nana 291 oblongata 291 pedicillata 291 petrosa 291 phaeosperma 289 pumila 291 purpurea 6, 281, 289, 291, 292, 294 rosea 289, 290 supina 289 uniflora 290, 292 varians 294 villosa 290 vogelii 282, 289, 290, 291 Terminalia 110, 207, 211, 237, 262 arjuna 211 bellerica 237, 262 catappa 237 ferdinandiana 110 oblongata 237 sericocarpa 237 Ternstroemia cherryi 237, 238 gymnanthera 238 tetracycline 270 tetrodotoxin 402, 403 Thargomindah 140 thiaminase 316, 317, 318, 319, 322, 335, 338 thiocyanate 411 Thylogale stigmatica 49 Thysanotus banksii 80 exiliflorus 80 tuberosus 80 Tinospora cordifolia 211 Ti-stem 97 Titan Arum 179 Tomatillo 156, 159, 166 tomatine 151, 152, 154,
155, 156 Tomato 5, 110, 136, 137, 138, 139, 143, 144, 145, 146, 147, 152, 155, 156, 164, 184 Tous-les-mois 65 toxalbumin 296 Toxicodendron diversilobum 208, 209 radicans 204, 205, 208 vernicifluum 209 Tradescantia paludosa 334 Tranes lyterioides 355 Trefoil Rattlepod 408 Treponema pallidum pertenue 280 Trianthema triquentra 81 Tribulus terrestris 116, 127 Trichocereus pachanoi 253 Trichodesmium 402 Trichosurus vulpecula 256 Triglochin dubium 81 triglochinin 414 trypsin 22, 88, 189 Turbina corymbosa 124 Turkey Red Oil 310 Turmeric 187, 302 Two-flowered Pea 409 Typha domingensis 81 Typhonium alismifolium 173 angustifolium 172 blumei 173, 174 brownii 172, 173 divaricatum 174, 176 flagelliforme 174 giganteum 173, 175, 187, 194 liliifolium 173 U Urtica dioica 53, 54, 57, 58 incisa 50, 53 urens 51, 52, 53 urushiol 6, 202, 203, 205, 206, 209, 210
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MEDICINAL PLANTS IN AUSTRALIA Volume 3 Plants, Potions and Poisons
V Valencia Orange 162 Vanilla Lily 81 Varanus varius 193 Velesunio ambiguus 319 Veratrum californicum 152 vibsanine A 239 Viburnum awabuki 239 Vicia faba 410 faba var. equina 410 faba var. major 410 faba var. minor 410 monantha 410 vicine 410 Vigna lanceolata 80, 81 radiata 80 vexillata 80 Villous Waterclover 322 Viscum album 305 viscumin 305 Vogel Tephrosia 282, 289, 290 volkensin 305 Voodoo Lily 180 W Waimakanui 323 Wall Rue 327 warburganal 238 Water Chestnut 81 Water Hyssop 322 Water Lettuce 321, 322
Water Pepper 238 Water Ribbon Yam 81 Water Spinach 99, 100, 101 Wattle seed 109, 110 Wedge-leaf Rattlepod 407 Weed Selenium Weed 110, 147, 257 West African Ebony 239 Western Poison Oak 205, 209 White Apple 236 White Ash 247 White Moonflower 102 White Siris 261 White Tephrosia 289 White Yam 182 Wild Bean 294 Wild Black Cherry 414 Wild Gooseberry 138, 140, 158 Wild Indigo 291 Wild Mango 226 Wild Passionfruit 110, 236 Wild Plum 110 Wild Quince 273 Wild Tomato 138, 139 Willie Wagtail 367 Winter Cherry 137, 159, 161 Wisteria floribunda 176 floribunda var. alba
176 Withania somnifera 127, 165, 211 withanolide 72, 165, 166 Wodji Poison 256 Wood Fern 328, 345 Woolly Cloak Fern 323, 324
Yellow Lily Yam 177 Yellow Morning Glory 121 York Gum 80 York Road Poison 255, 256 Yoruba Indigo 280 Youlk 107
X Xango 229 Xanthorrhoea 43, 368 Xanthosoma jacquinii 188 robustum 188 sagittifolium 176, 187, 188, 189 violaceum 188
Z Zamia angustifolia 369 boliviana 357 fischeri 394 furfuracea 357 integrifolia 356, 357, 370, 371, 394 kickii 368 loddigesii 369 paucijuga 369 pumila 356, 369, 370 spiralis 372, 376 vezquezii 369 Zamia Palm 368, 387 Zamites feneonis 349 Zantedeschia aethiopica 192 Zanthoxylum armatum 54, 231 Zea mays 65, 334 zeaxanthin 144, 145, 146, 147, 148, 149, 222 zeta-carotene 144 Zizyphus mucronata 302
Y Yam 5, 65, 79, 84, 85, 86, 176, 197 Desert 103 Five-leaf 87 Grass 82 Greater 87, 88, 91, 92, 93, 96 Hairy 88 Long 79, 80, 81, 86, 87 Potato 89, 96 Yam Daisy 84 Yautia Palm 188 Yellow Butterfly 335 Yellow Gentian 230
