A Review on Avian Anatomy

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

A Review on Avian Anatomy R M Arriza, C G Buscato, C M Butil, P G Espina, R T Leonida Abstract—The evolution of flight has endowed birds with many physical features in addition to wings and feathers.Birds have a light skeletal system and light but powerful musculature which, along with circulatory and respiratory systems capable of very high metabolic rates and oxygen supply, permit the bird to fly. The development of a beak has led to evolution of a specially adapted digestive system.All information were gathered from books and online articles. Keywords—anatomy, aves, avian anatomy, bird, comparative vertebrate anatomy, vertebrates

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1 INTRODUCTION

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ves are feathered, endothermic, winged, bipedal, and egg-laying vertebrate. Their evolutionary origins are amongst the reptiles. Fossil records indicate that birds most likely arose from a group of archosaurs called thecodonts during the Jurassic period (Prum, 2008). They are members of Maniraptora (Gregory, 2002), a group of therapods which includes dromaesaurs and oviraptorids. Birds are the only clade of dinosaurs to have survived the Cretaceous-Paleogene extinction event 65.5 million years ago. They are considered to be the modern descedants of dinosaurs (EOL). Feathers, beak having no teeth), egg-laying, lightweight skeleton and high metabolic rates are the characteristics of modern birds. There forelimbs were modified to wings. Birds have reduced weight. They have hollow, stutted, spongy bone (pneumatic). Their feathers are lightweight and yet well adapted for aerodynamics and insulation. Fused bones are evident (appendages and girdles) which provide rigidity to the skeleton. Birds also have reduction in bones, e.g. teeth. Birds‘ entire anatomy and physiology is adapted for efficient fligh, but not all birds are capable of flight. Most birds are morphologically very similar because they are constrained by the demands of flight (Swanson). Birds have light skeletal system (pneumatized bones), light and powerfull musculature, amd high metabolic rates. In the tenth edition of the 'SystemaNaturae' (1758), the first work in which the species concept is consistently applied, Linnaeus enumerates 564 species of birds, known to him from all parts of the world. In the subsequent 150 years a number of additional counts were published, each one to be quickly superseded by a newer one.Sharpe (1909) estimated the total bird species to be about 18, 900 species. According to Mayr (1935), Sharpe treated all subspecies as full species and that the actual number of species of birds must be considerably below Sharpe‘s figure. Mayr (1935; 1946) estimated and arrived at the figure 8,500 species. To date, there are about 10,000 species of birds recorded. Birds are sensitive to habitat change, and therefore, they are considered to be one of the indicators of environment health (Gregory et al., 2003). Changes in bird populations are often the first indication of environmental problems. Whether ecosystems are managed for agricultural production, wildlife, water, or tourism, success can be measured by the health of birds (Gregory et al., 2005). About 120 - 130 species have become extinct as a result of human activity since the 17th century, and hundreds more

before then. Currently about 1,200 species of birds are threatened with extinction by human activities, though efforts are underway to protect them.

2 BIRD ANATOMY 2.1 General Morphology Most birds can fly;their foremlimbs are modified into wings; which distinguish them from almost all other vertebrate classes. Birds have scaly legs and feathers (Menon et al, 1996; Spearman and Hardy, 1985). Feathers are highly modified scales, and are important in several ways. Soft down feathers trap still air close to the surface of the body, thermally insulating a bird. Contour feathers on the body establish the smooth, streamlined contour of a bird's body, and the enlarged flight feathers form the aerodynamic surfaces of the wings and tail.Featherless areas, the beak and feet, are covered with relatively thick, heavily cornified epidermis: rhamphoteca on the beaks and podotheca on their feet (Lucas and Stetteheim 1972). These cornified cells produce beta-keratin and thecalcium deposited between keratin proteins generally make this covering hard and strong (Homberger and Brush, 1986: Bonser, 1996). Birds also come in different colors. Among birds with colorful skin, the coloration is due either to pigments, structural mechanisms in the epidermis, or to blood in the superficial capillary network (Lucas, 1970; Prum and Torres, 2003). Claws are found at the distal end of all toes of all birds and cover the bones of terminal phalanges. The dorsal portion of claws is highly keratinized and calcified and is very hard. Claws care curved to varying degrees, relative length, and pointedness (Stettenheim, 2000). Flight is the primary means of locomotion for most bird species and is used for breeding, feeding, and predator avoidance and escape. 2.2 Integumentary System Birds have thinner epidermis, the most superficial layer of the skin, than mammals comparable size, flexible, and smooth, and this is due, at least part, to selective pressures to minimize body weight for more efficient flight (Spearman 1966). The epidermis is thinnest in areas covered by feather and thickest in exposed, featherless areas, including the covering of the beak (rhamphotheca) and feet (podotheca). The reticulate scales (papillae) on the underside of the toes and the distal end of the tarsus are formed into thick pads to withstand compres-

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

sion, especially in terrestrial species. The pads underlie the joints and are separated by transverse furrows or gaps, which open and close as the toes are bent (Lennerstedt, 1975). The epidermis has two main layers (Figure 1) – a superficial stratum corneum (consists of flattened, keratinized cells) and a deeper strateusgerminativium. The stratum corneum can be viewed as having a ‗brick-and-mortar‘ organization, with the keratin-enriched cells forming the ‗bricks‘ and the extracellular lipids the ‗mortar‘ (Elias and Menon 1991). However, compared to reptiles and even mammals, cells in the stratum corneum have less keratin and, as a result, this barrier is less stringent and can facilitate evaporative cooling while retaining the capacity for facultative waterproofing (Menon et al. 1996).

Fig 1.Cross-section through the skin of a bird or mammal (From: Lillywhite 2006).

The high body temperatures of birds, increased heat production during flight, insulation by plumage and the lack of sweat glands, require a higher rate of evaporative cooling through a relatively "leaky" epidermal permeability barrier. Besides forming a dynamic barrier that regulates water loss through the skin, epidermal lipids may also have antimicrobial properties and offer protection against ultraviolet light (Menon 1984). Birds‘ integument is also modified to function in skin coloration. Generally, patches of bare skin, other than the bill and legs, can be found in birds belonging to at least 19 different orders and 62 families (Negro et al. 2006). The coloration is due either to pigments, structural mechanisms in the epidermis, or to blood (and, specifically, hemoglogin in the red blood cells) in the superficial capillary network (Lucas 1970, Prum and Torres 2003). Colored unfeathered areas on the head and necks of birds may be important in (1) intra- and intersexual communication, e.g., advertising status or quality, (2) thermoregulation, and (3) preventing the soiling of feathers for species that sometimes extend their heads into carcasses when feeding (e.g., vultures and condors). Claws are found at the distal end of all toes of all birds and cover the bones of terminal phalanges. Some birds also have wing claws. The dorsal portion of claws is highly keratinized and calcified and is very hard. Claws are curved to varying degrees, relative length and pointedness (Stettenheim, 2000). Glen and Bennett (2007) examined claw morphology and placed terrestrial birds into six categories, with grounddwelling birds having longer, less recurved claws and the amount of curvature increasing for birds that are increasingly arboreal in their foraging habits (Figure 2). Among raptorial birds that use their feet to capture and kill prey, claws (also called talons) are relatively long, highly recurved, and pointed.

Fig 2. Categories (GB, Gg, Ga, Ag, Aa and V) of avian toe claws based on the degree of ground foraging; GB= ‘ground based’, limited to foraging on the ground; Gg = ‘dedicated ground foragers’; Ga = ‘predominantly ground foragers’; Ag = ‘predominantly arboreal foragers’; Aa = ‘dedicated arboreal foragers’; V = ‘vertical surface foragers’. Analysis of the toe claws of 249 species of birds revealed that claw curvature increases as tree foraging becomes more predominant (From: Glen and Bennett, 2007).

Bird bills consist of bones that form the cores of the upper and lower mandibles. However, the outer surface and part of the inner surface of these bones are covered with a modified integument called the rhamphotheca (Figure 3). The epidermis of the rhamphotheca is relatively thick, hard, and consists of heavily cornified cells (Lucas and Stetteheim 1972).

Fig 3.A sagittal section near midline of the upper beak of a 2-week-old domestic chicken. The bill tip is to the right.The dorsal region shows the upper smooth portion of the bill covered by the rhamphotheca (Rh). Beneath the rhamphotheca is the epidermis (Ep) that provides a constant supply of cellular material to form the outer, hardened covering of the beak. Internal to the epidermis is the dermis (Dr) layer that is the most heterogeneous of all tissue layers. It extends from the epidermal to bone layers (Bn) (From: Kuenzel 2007).

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Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

These cells produce beta-keratin like that found in avian scales and claws and calcium deposited between the keratin proteins generally make the rhamphotheca hard and strong (Homberger and Brush 1986, Bonser 1996). The epidermis is tightly bound to bone by a thin dermal layer that contains numerous collagen fibers. The dermis also contains sensory receptors, including Herbst and Grandry corpuscles that are sensitive to touch and vibration. The integument of the bill grows continually from the base and culmen, with growth directed rostrally so that there is continuous movement of the horny beak from base to tip. The rhamphotheca, particularly at the tomia, is worn away by abrasion from food and other materials and by friction where the upper and lower bills meet. In some birds, including raptors (Falconiformes), owls (Strigiformes), parrots, cracids, and pigeons, the rhamphotheca at the base of the upper bill is called the cere (Figure 4; Stettenheim, 1972). The cere is a thickened, often brightly colored portion of the integument that straddles the base of the nasal region. (Lucas 1979). Lucas and Stettenheim (1972) suggested that the cere may provide protection for the underlying elongated nasal fossa (cavities).

Fig 4.Lateral view of the rock pigeon skeleton.Note the many fused bones along the axial skeleton (skull, spinal column, and pelvis). The fused bones provide a strong, stable central platform for the flight muscles. Note how light the bird’s skeleton is; in some birds the skeleton weighs less than the feathers (From: Proctor and Lynch, 1993).

Fig 3. The cere (C) of a Rock Pigeon located at the base of the upper bill. The arrow points to the external nares; (O), operculum (a small disc of cartilage centered in the nostril that keeps foreign objects out of the nasal cavity) (From: Purton 1988).

2.3 Skeletal System One of the requirements of heavier-than-air flying machines, birds included, is a structure that combines strength and light weight. Birds have evolved a number of modifications to their skeletal system, including pneumatic, or hollow bones, and reduction of the number of bones by loss or fusion. Hollow, air-filled bones lighten the weight of the skeleton. Skeletal adaptations lend strength to the skeleton (Figure 4) so that the thrust (forward force) generated by the wings can lead to maximal lift, and the bird can be propelled through the air with minimal compression to the body cavity. Some of the vertebrae and some bones of the pelvic girdle of birds are fused into a single structure, as are some finger and leg bones -- all of which are separate in most vertebrates. The skeleton of birds is remarkable for the rapidity of its ossification and the light and elegant mechanism displayed in the adaptation of its several parts.The osscous substance is compact, and exhibits more of the laminated and less of the

fibrous disposition than in the other vertebrate classes. This is more especially the case in those parts of the skeleton which are permeated by the air (Figure 5). The bones which present this singular modification have a greater proportion of the phosphate of lime in their composition than is found in the osseous system of the mammalia, and are whiter than the bones of any other animal (Owens, 1866).

Fig 5.The hollow inside of a bird's ulna. While maintaining strength, most of the bones are pneumatic, meaning they are hollow and filled with air spaces connected to the respiratory system.

Birds have many bones that are hollow (pneumatized) with criss-crossing struts or trusses (Figure 5) for structural strength. The number of hollow bones varies among species, 3

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

though large gliding and soaring birds tend to have the most. Respiratory air sacs often form air pockets within the semihollow bones of the bird's skeleton (Gary, EKU). Flight adaptations found in most birds can easily be seen in their skeletal structure. The modifications of the sternum of birds relate to their faculty of flight; more directly, to the adequate origin of the muscles acting upon the pectoral limb, less directly to the mechanism of respiration needed by the conditions of the lungs (Owens, 1866). The sternum of the bird (Figure 6)is the bony ventral wall of the trunk. The posterior margins of the sternum are used as a taxonomic character. There may be one or two notches or holes (fenestrae) or nothing at all. The sternum, or breastbone, bears a prominent keel where the flight muscles attach (Figure 6).The keel runs axially along the midline of the sternum and extends outward, perpendicular to the plane of the ribs (Cummins, 1996).In order to afford origin to the accumulated fasciuli of the pectoral muscles, which other wise would become blended together over the

Fig 6.Topography of the breastbone. 1-Spinaexterna; 2-Labium ventrale; 3-Labium dorsale; 4-Crista sterni (or keel); 4a-Anterior pillar; 5-Apex cristae sterni; 6-Metasternum; 7-Facets for the ribs; 8-Processuslateralis; 8aLateral sternal notch; 9-Processusintermedius; 9a-Medial sternal notch.

middle of the sternum, this osseous crest is extended downward, analogous to the cranial crest which intervenes to the temporal muscles in the carnivorous mammalia; and which; in the like manner, indicates the power of the bite. The keel varies in depth, length, contour of the front and lower borders, and degree of production, freedom, or otherwise of the angle between those borders (Owens, 1866). Keels do not exist on all birds; in particular, some flightless birds lack a keel structure. The breastbone is consists of a convex/concave basal plate (Figure 6) and the keel perpendicular to it, protruding ventrally. From the breastbone, two coracoids form the connection to the shoulder, articulating to the breastbone in the slot between the Labium ventrale and dorsale. The furcula is attached to the apex of the keel by a ligament or is fused to the apex in Frigatebirds and Pelicans. The ribs are connected to each side of the breastbone by small flexible ligaments.

Fig 7.Avian pectoral girdle.Sternum; keel/carina; Coracoid; Clavicle / Furcula; Scapula; sternal notch; Foramen trioceum / trioseal canal.

The furcula, a fused clavicle (collarbone), serves as a brace during the flight stroke; it's visible as a large Y-shaped bone (Figure 7) ahead of the sternum. The clavicle is also found in non-avian dromaeosaurian dinosaurs, and was probably coopted in function from the dromaeosaurian function of providing a brace for the shoulder girdle while holding prey.In conjunction with the coracoid and the scapula, it forms a unique structure called the triosseal canal, which houses a strong tendon that connects the supracoracoideus muscles to the humerus. This system is responsible for lifting the wings during the recovery stroke (Frank, 2007; Proctor et al., 1998). Crucial for bird flight is a canal formed by the articulation of the humerus (forewing bone), the scapula (shoulder blade), and the coracoid (bone connecting the sternum itself to the humerus). Through this canal, the foramen triosseum or triosseal canal (Figure7;), runs the tendon of the supracoracoideus muscle, which attaches to the sternum and the dorsal side of the humerus, and lifts the wing upwards in flight. The powerful downstroke of the wing is powered by the large pectoralis muscles, which also attach to the sternal keel.

Fig 8.Atlas (A) and axis (B) of a Common Buzzard (Buteobuteo). A: 1 vertebral arch, 2 - glenoidal cavity for occipital condyle of skull, 3 - ventral process, 4 - transverse process, and 5 - lateral vertebral notch. B: 1 dens, 2 - articular facet for atlas, 3 - vertebral foramen, 4 - transverse process, 5 - spinous process, 6 - postzygapophysis, 7 - vertebral canal (From: Bitoiu et al. 2011). 4

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

The vertebrae comprise five groups (Figure 4). (1) The cervicals(Figure 8) extend from the skull to the first vertebra with a complete rib reaching the sternum. There may be 13 - 25 in birds. (2) The five thoracic vertebrae bear complete ribs (Figure 8). (3) The three lumbar vertebrae, (4) four sacral and (5) six of the twelve caudal vertebrae are fused with the pelvis into the synsacrum. Note that the transverse processes of these vertebrae can be seen within the synsacrum. The last six caudal vertebrae are unfused. The last one is a fusion ancestrally of several vertebrae and is called the pygostyle. It bears the tail feathers. As the prehensile functions of the hand are transferred to the beak, so those of the arm are performed by the neck of the birdl; the cervical vertebrae (Figure 9) is therefore composed of numerous, elongated and freely movable vertebrae, and is never so short or so rigid but that it can be made to apply the beak to the coccygeal oil-gland, and to every part of the body for the purpose of oiling and cleansing the plumage (Owens, 1866). Note the first two vertebrae, the specialized atlas and

Fig 10.Thoracic vertebrae of birds.(A) Anterior view (B) Posterior view (C) Lateral view.

is the only structure used to manipulate objects, such as food items, the vertebrae of the neck must be highly flexible. The high degree of flexibility is made possible by the heterocoelous condition of the centrum of each vertebra. The anterior articular surface is convex dorsoventrally and concave from side-to-side. The posterior surface is the reverse. Thus, the articulation between vertebrae is similar to two saddles fitted together.The dorsal vertebrae are shorter than most of the cervicals, and with broader neural arches, in consequence of the greater development of the transverse processes; but their bodies become much compressed, and in some birds are reduced to the form of vertical laminae towards the sacral region (Owens, 1866).

Fig 9.Cervical vertebrae of birds. (A) Posterior view of cervical vertebrae with transverse foramina, the heterocoelous centrum & postzygapophyses. (B) Bird dorsal view of cervical vertebrae showing the short neural spine & pre-zygaphyses to the left.

axis (Figure 8). The atlas is ring-shaped and forms a ball-andsocket joint with the occipital condyle on the occipital. It rotates on a process of the axis. The two speedily effect a partial coalescence; the body of the first, e.g. as an ―odontoid process‖ to that of the second, and usually presenting a pair of small facets to articulate with its own neurapophyses, which are mainly supported by the hypaphysis simulating the entire centrum of the atlas. The centrum of the axis is sometimes carinate below with a slight posterior production. The thoracic vertebrae of birds (Figure 10), and vertebrae other than those located in the neck region, are fused to help keep the trunk of the body stiff during flight. Because the bill

Fig 11.Thoracic, synsacrum, caudal, and pygostyle.Notarium, synsacrum, and Oscoaxae of the turkey, Meleagrisgallapavo; ventral view.(From Harvey et al., 1966).

The bones of a bird's pelvic girdle and the lumbar, sacral, 5

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

and a few caudal vertebrae are fused into a single, solid structure called the synsacrum. Additionally, through the fusion of these bones, shock incurred from the force of the beating wings is transferred to the air.

The wing (Figure 15) has several fused and missing elements from the basic vertebrate limb. The humerus is the stout bone connected to the shoulder. Note the small opening at the proximal end through which the cavity within the bone is connected to an air sac inside the body. At the distal end the humerus widens to create two surfaces which articulate with the ulna and the radius. The ulna is the stouter and more curved; the radius is the more slender.

Fig 12.Avian pelvic girdle. The two "scooped" areas near the top are the crests of the ilium, the line down the middle is the fused vertebrae (synsacrum), and the center of the bottom is the start of the tail.

Avian ribs are broad, flat, and lie close enough together to prevent much compression. In addition, each rib overlaps the next due to an uncinate process. The uncinate processes (Figure 13) provide additional strength to the rib cage encasing the bird's vital organs and further restrict movement between vertebrae as well as serving for muscle attachment. Some of the first ribs (the first two in pigeons) do not attach to the sternum. Note that the ribs are in two segments, the vertebral ribs and the sternal ribs. On the vertebral portion of all but the first and last ribs is an uncinate process - a tab-like projection.

Fig 14.Avian forelimb.It forms tripod of bones and has modified forelimbs which folds against the body in Z-shape for compactness.

In birds the humerus (Figure 14) has a smooth shaft, subelliptic in transverse section, with expanded ends, the proximal one being the broadest. Lengthwise the bone gently sigmod, the proximal half being convex palmad, the distal half concave, with the plane of the terminal expansions vertical, as the bone extends along the side of the trunk from its scapulacoracoid articulation backward, in its position of rest (Owens, 1866). The radius (Figure 14, 15) is always the more slender bone of the two, sometimes in a remarkable degree; its proximal end is expanded, subelliptic, with a concavity for the oblique

Fig 13.Avian ribs. The overlapping processes (or uncincate process) provide some rigidity to the rib cage as well as serving for muscle attachment.

The pectoral girdle (Figure 7) consists of three pairs of bones: The scapulas, the flat bones lying on the dorso-lateral surface of the ribs; the coracoids, the stout bones which brace the shoulder against the sternum; and the clavicles, which fuse anterior to the sternum to form the furcula (wishbone).

Fig 15.Right forelimb of I Pigeon, II Archaeronissiemensis, drawn by the author from the fossil in Berlin; H humerus, R radius, U ulna, c centrate, d 1-3 first to third digits, I intermediu, mc 1-3 first to third metacarpals, r radiale, u ulnare, 1+2 coalesced first and second distal carpals.

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Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

tubercle, and a thickened convex border next to the ulna for articulation with that bone: a little beyond that articular expansion is the tubercle for the insertion of the biceps. The ulna (Figure 14, 15) is straight or with a single and slight curve, more marked in the shorter antibrachium of Gallinaethan in the long one of the long-winged waders and swimmers. The proximal end is most expanded, and is obliquely truncate for the articular excavation adapted to the ulnar tubercle of the humerus; the obtuse angular production of the ulna, behind or anconad of the cavity, represents in different degrees in different birds the olecranon, but is always short: an extension of the bone radiad is obliquely excavated for the head of the radius. The distal end of the ulna slightly expandsinto a trochlear joint very convex from the radial to the ulnar side, rather concave from the anconal to the palmar side, and this chiefly at, the ulnar part of the trochlea. Notice the bumps on the ulna (Figure 16). These bumps help support attachment of the secondary flight feathers, which provide lift. The bones of the hand are developed in length, but contracted in breadth. The wedge-like adjustment of the free carpals is such as to restrict the movements of the hand upon the arm to abduction and adduction, or flexion in the ulno-radial plane, requisite for the outspreading and folding up of the wing. The hand of the bird moves thus in a state of pronation, without the power of rotation or of proper flexion or extension so that the wing strikes firmly and with the full force of the drepressor muscles upon the air (Owens, 1866).

Fig 16.Bumps on the ulna. The photo at top creates an optical illusion. To make the bumps stand out in a photograph, the bone was held nearly parallel to the sun’s rays, so sunlight would cast a shadow. That added depth to the flat image. The light was coming from the right side, so the bright area is the bump and the dark area to the left is the shadow. Without knowing this, and presuming the light is coming from the left in the photo, it looks like a hole with the right border of the pit reflecting light (HSU).

The pelvis (Figure 12) is a fusion of the three pelvic bones shared by all vertebrates: ilium, ischium, and pubis. On the lateral surface is a socket, the acetabulum, for the attachment of the femur. All three bones meet at this point. The ilium is the dorsal part of the pelvis. It is dorsally concave anteriorly

and convex posteriorly. It is fused with the transverse processes in the synsacrum. The ischium is the thin bone extending ventrally from the ilium and forming the side of the pelvis. The opening in the side of the pelvis is along the line of fusion of the ilium and ischium. The pubis is the thin rodlike bone. The femur (Figure 17) has a cylindrical shaft, which when not straight, is slightly bent forward. It is always shorter than the tibia. The head is hemispherical, proportionally small, and largely scooped out above for the round ligament which fills up the vacuity in the acetabular wall: it is sessile, with its axis nearly at right angles to that of the shaft. The tibia (Figure 17) is the chief or the longest bone of the hinlimb, showing its extreme character in this respect in most Stilt-birds. The shat is straight and mainly subtriedal, expanded at both ends and most so at the upper one. This presents a semi-oval surface not quite transverse to the shaft, but with the truncate margin raised toward the fore part of the bone, and more or less developed above the level of the undulating articular part. The fibula (Figure 17) is a styliform bone ending in a point below at various distances down the tibiain different bids. The articular head is subcompressed, convex in the longer axis, slightly curved backward, hollowed on the inner (tibial side): rather convex externally: the shaft show rough linear tract for the attachment to the tibia: and there are sometimes tuberosities for tendinal insertions on the opposite side (Owens, 1866). The lines of demarcation between individual bones of the

Fig 17.Avian hind limbs. The legs also exhibit fusion and reduction or loss of parts. The femur has a prominent head which fits into the acetabulum.The fibula is much reduced and exists only as a splinter bone partly fused to and lying parallel to the tibiotarsus.The tibiotarsus is a fusion of the tibia at its distal end with some tarsal elements.The other tarsals are fused with a fusion of the second, third, and fourth metatarsals to form the tarsometatarsus. Remnants of the three metatarsals are visible at the distal end where they articulate with the toes.

skull are nearly impossible to see in adult birds because of fusion that accompanies ageing. The skull (Figure 18) can be divided into three groups of bones: cranium, face, and tongue. The cranium encloses the brain and constitutes the post7

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

erior part of the skull. The occipital forms the base or rear

Fig 18.Avian skull. (A) and (C) Lateral view (B) Dorsal view of the skull. From the side, the skull shows how much the eyes dominate the avian head. To accommodate the large orbits the brain has been forced down and back into the occipital region and now tilts in th skull at an almost 45º angle. Note how open the bird’s skull is. Composed largely of tiny struts and paper-thin sheets of bone, the structure is remarkably strong (Proctor and Lynch, 1993).

portion of the cranium. The large opening in the base of the bone is the foramen magnum. The spinal cord connects to the brain through this foramen. The back and posterior part of the brain case are formed by a medially fused pair of squarish bones, the parietals. Anterior to the parietals is another pair of bones, the frontals, which form the roof of the skull and the orbit (eye socket). Lateral to the frontals and parietals on each side of the head are the squamosals. They form the sides of the brain case and the posterior margins of the orbits. The ear opening lies under the lower edge of the squamosal (Proctor and Lynch, 1993). The floor of the brain case is formed by part of the sphenoid. Viewed ventrally, the sphenoid is roughly triangular in shape with the base attached to the occipital and the apex projecting anteriorly. This projection, the basisphenoidal rostrum, forms the central axis of the base of the skull. The base of the sphenoid (basisphenoid) lies beneath a membranous bone, the basitemporal plate. The basisphenoid also projects laterally to form the anterior border of the ear opening and connects with the sphenoid to form part of the brain case and the lower posterior and inner walls of the orbits up to and including the rear margin of the optic foramen, the opening in the rear of the orbit for the optic nerve. Additional parts of the sphenoid extend forward and upward from the optic foramen to form the central part of the interorbital septum - a thin vertical plate separating the orbits. In some birds, the septum is incomplete, with one or more openings between the orbits. Extending forward from the sphenoid to the nasal cavities is the ethmoid, a perpendicular bone which completes the interorbital sep-

tum. It extends from the frontal bones ventrally to the rostrum. Anteriorly, a pair of lateral plates of the ethmoid forms a septum separating the orbits from the nasal cavities. A small portion of the ethmoid extends anteriorly beyond the septum to separate the two nasal cavities. The face is composed or are directly associated with the upper and lower mandibles (the maxilla and dentary). The quadrate, a quadrangular bone with a central constriction, connects the squamosal and sphenoid with the lower mandible, zygomatic bar, and pterygoid. The quadrate is one of the kinetic (movable) bones of the skull; the articulation at each end is free. A slender zygomatic bar lies below each orbit. The quadratojugal makes up most of the bar and is connected to the quadrate. The much smaller jugal lies at the anterior end of the bar and is fused to the maxilla. The maxilla forms the posterior part and side of the upper mandible and part of the palate. It connects with the jugal posteriorly, palatine ventrally. Since the right and left halves do not connect medially, the palate is cleft. The two premaxillae fuse anteriorly to form the tip of the upper mandible. Each premaxilla has three posterior projections. (1) One helps to form the culmen (the upper ridge of the beak) by fusing with its equal on the other side; it extends back to the frontal. (2) Another extends horizontally to the maxilla and forms half of the tomium (cutting edge of the bill). (3) Part of the palate is formed by the third process which extends along the roof of the mouth to meet the palatine. Each of the nasals forms the posterior border of the external nares (nostril) by splitting into two processes; a medial one projects forward to join a process of the maxilla. Posteriorly the nasals fuse with the frontals and medially with each other; ventrally they rest on the ethmoid. Another pair of bones dorsally visible from the anterior margin of the orbit; the lacrimals, are small flattened bones extending from the frontals and nasals downward to the zygomatic bar (Proctor et al., 1998). The tongue is supported by the hyoid apparatus or hyoid bone. Three bones linearly arranged comprise the central element of the hyoid. The tongue is supported on the anterior most element of this core, aided by a piece of cartilage projecting forward from that element. Two horns project from the central axis. Three bones make up each horn.

Fig 19.(a) Skull of Great Spotted Woodpecker, (b) hyoid apparatus of a Great Spotted Woodpecker, and (c) hyoid apparatus of a non-woodpecker (Eurasian Hoopoe) (From: Wang et al. 2011).

To project the tongue, the bird slides the hyoid forward. Upon retraction, the horns, encased in a muscular sheath, slide backward behind the skull. In woodpeckers (Figure 19), the horns even curve forward over the top of the skull and down onto the forehead. 8

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

2.4 Digestive System The digestive system of birds is adapted to the demands of flight. Birds consume more food in proportion to their size than most animals. As a group, birds consume just about any type of food you can imagine, including amphibians, ants, buds, carrion, crustaceans, fish, fruit, grass, insects, larvae, leaves, molluscs, nectar, other birds, pollen, reptiles, rodents, roots, sap, seeds, suet, snails, wax, & worms. To meet their metabolic needs while remaining as light as possible (to be efficient flyers), the digestive system of birds has to be both as light as possible and as efficient as possible. Weight has been minimized by the loss of teeth &, in many birds, limited jaw musculature. The major components of the avian digestive system (Figure 4)are the alimentary canal plus several accessory structures. The 'canal' includes the oral cavity, pharynx, esophagus (which includes a crop in some birds), stomach (proventriculus& gizzard), small intestine, & large intestine. The large intestine then empties into the cloaca. Important accessory structures include the beak, salivary glands, liver, & pancreas.

ventrolaterally on the anterior tongue (Iswasaki, 2002). Birds do have a tongue, but unlike mammals, the avian tongue has a bone in it (Figure 5). The avian tongue is narrow, pointed and contains little intrinsic muscle.Its morphology varies with food habits (e.g. fish-eating species (like commorants) typically have small, undifferentiated tongue because fish are often swallowed whole). Hummingbirds have tongues that act like a fluid-trap (Rico-Guevara and Rubega, 2011);nutcrackers have a unique structure on the anterior part of the tongue and are efficient in shelling seeds (Jackowiak et al. 2010); woodpeckers have long, extensible, and barbed tongue which facilitate the capture and extraction of prey from bark crevices (Wang et al. 2011).

Fig 21: Dorsal view of the surface of the lower bill of a Great Cormorant (Phalacrocoraxcarbo). Arrow shows the tongue with sharpened tip. 1, hyoid bones; 2, laryngeal sulcus with ostium; 3, esophagus. Scale bar, 12 mm. (From:Jackowiak et al. 2006)

Although not part of the digestive system in an anatomical sense, some birds, like hawks and owls, use their feet and talons to capture prey. Typically, raptor preys are killed by the talons of the contracting foot being driven into their bodies; if required, the hooked bill is used to kill prey being held by the talons.

Fig 20.Typical avian digestive system.Oesophagus; crop; liver; proventriculus; gizzard (ventriculus); pancreas; intestine; and cloaca.

A bird's bill consists of a bony framework covered by a tough layer of keratin. The keratin layer is continuously replaced throughout the life of a bird & is just as continuously worn down by eating and manipulating hard objects. The cutting edges of the beak are the tomia. The bill plays a critical role in food acquisition &, of course, bill morphology varies with food habits. Birds‘ oral cavity contains few mucous glands and taste buds. Salivary glands are well-developed in manybirds but are reduced in aquatic species (because aquatic preys like fish require little additional lubrication to be easily swallowed). The taste buds of birds may be located in the upper beak epithelium, in the anterior mandible, and the mandibular epithelium posterior to the tongue. Some taste buds are also located

Fig 22.(from left –right) Harpy Eagle, Golden Eagle, Bald Eagle, Great Horned Owl, Red-tailed Hawk, & Peregrine Falcon.

The esophagus is large in diameter, particularly in birds that swallow large meals (e.g., cormorants, herons, & raptors). Swallowing is accomplished by esophageal peristalsis, and in most birds appears to be aided by extension of the neck. It may also serve as temporary storage of food (temporary distension - fish-eating species, birds of prey & some fruit eaters 9

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like Cedar Waxwings. Most but not all birds have a crop, which varies from a simple expansion of the esophagus to one or two esophageal pouches. Crop is an out-pocketing of the esophagus that's particularly well-developed in seed-eaters like pigeons & doves (Columbiformes) and gallinaceous birds (grouse and pheasants). Depending on the state of contraction of the stomach, food being swallowed is diverted into the crop, then later propelled into the stomach by waves of peristalsis in the crop. The crop is also specialized for production of 'milk' (Figure 23) that pigeons & doves feed to their young. Crop 'milk' is rich in proteins, fats, & vitamins and is produced by proliferation & sloughing off of epithelial cells that line the crop.

Fig 23.The non-‘lactating’ pigeon crop (A) has a completely different appearance from that of the ‘lactating’ crop (B). The lactating crop is more than twice the size of the non- ‘lactating’ crop, with a thickened wall and two very obvious lateral lobes. When the ‘lactating’ crop is opened (C) the pigeon ‘milk’ is seen as a bed of close-packed discrete rice-shaped pellets that are closely associated with the mucosal surface of the tissue (From: Gillespie et al. 2011).

Both male and female Rock Pigeons (Columba livia) produce pigeon ‘milk’ that is fed to their young. Pigeons generally lay two eggs one day apart, which hatch 18 days after they are laid. Two days before the first egg hatches, pigeon ‘milk’ begins to be produced in the crop of the parent birds. A similar substance is produced by flamingos and male Emperor Penguins. The normal function of the crop is food storage. During the process of pigeon ‘lactation’, a curdlike substance is regurgitated from the crop and fed to young pigeons. This 'milk’ is 60% protein and the remainder is mostly fat (32-36%) with a small amount of carbohydrate (1-3%), in addition to the mineral (calcium, potassium, sodium, and phosphorus) content. Pigeon 'milk' also contains IgA antibodies and antioxidants (carotenoids).

Fig 24.Avian stomach.The glandular stomach receives food from the esophagus, and secretes mucus, HCl and pepsinogen, similar to what is seen in the mammalian stomach. The gizzarddo the grinding.

Birds have a glandular stomach, or proventriculus, and muscular stomach or gizzard.Proventriculus(Figure 24) receives food from the esophagus & secretes mucus, HCl, and pepsinogen. HCL and pepsinogen are secreted by the deep glands (Figure 25). Pepsinogen is converted into pepsin (a proteolytic, or protein-digesting, enzyme) by the HCl.

Fig 25.Photomicrograph (50X) of a cross section through the proventriculus showing folds of mucous membrane (P); deep proventricular glands (GP); capsule (connective tissue) around the glands (arrow head); muscle layer (m); serosa (connective tissue) with blood vessels (S), and the lumen (L) (From: Catroxo et al. 1997).

The gizzard (Figure 24) is a disk shaped, very muscular (but less so in birds that eat meat, insects, nectar, and other 'soft' foods)and in many birds contains small stones (in seedeating birds, contain grit) that facilitate grinding of foodstuffs. It is the avian equivalent of teeth.

Fig 26.(1) Section through inner lining of a chicken gizzard. A, koilin, B, crypts, C, glands that secrete koilin, D, epithelial surface, E, desquamated epithelial cells,(2) Mucosa of the gizzard. A, koilin, B, secretion in gland lumens and crypts, and (3) Koilin layer. A, secretion column, B, koilin-layer surface,C, horizontal stripe indicating a 'pause' in secretion of the koilin, D, cellular debris. (From: Eglitis and Knouff 1962).

One of the gizzard's two orifices receives ingesta from the 10

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glandular stomach and the other empties into the duodenum. The gizzard is lined with a tough, abrasive keratin-like layer of koilin, known as the cuticagastrica (or cuticle; Figure 26). The cuticle is secreted by simple tubular glands (Figure 27). Grinding action may, particularly in seed-eating birds, be assisted by grit and stones deliberately ingested.

Fig 27. Photomicrograph (210X) of longitudinal section of the gizzard showing folds of mucous membrane lined by simple prismatic epithelium (P); simple tubular glands (Gs) in the lamina propria constituted by connective tissue (Lp); secretion of glands (S) that are continuous with the cuticle (or koilin); (C), part of muscle layer (m), interpersed with bundles of connective tissue (Tc) (From: Catroxo et al. 1997).

Fig 28.Ostrich (Struthiocamelus) stomach. Note how particle size of material in the gizzard (ventriculus) is smaller than in the proventriculus due to the grinding action of the muscular walls plus small pebbles (gastroliths). The capacity to reduce particle size is related to the metabolic demands of a species. Therefore, particle size reduction is often considered the key digestive difference between ecto- and endotherms that allows endotherms to rely on shorter digesta retention times without losing digestive efficiency, and hence facilitate the high level of food intake necessary to meet their increased metabolic requirements. Oes, esophagus; Prov, proventriculus;Gizz, gizzard; SI, small intestine (From: Fritz et al. 2011).

The avian gastrointestinal tract, unlike that of mammals, executes distinct reverse peristaltic movements that are critical to optimal digestive function (Duke 1994). The gastric reflux

allows material in the gizzard to reenter the proventriculus for additional treatment with acid and pepsin. A gizzard system is advantageous (Figure 28) when the organismal design demands that the site of particle size reduction be close to the center of gravity; as such, the use of a gizzard is usually linked to the primary characteristic of herbivorous birds, flight. In contrast, adaptations for chewing intrinsically increase the weight of the head. The use of the gizzard system has the potential advantages that intake rate is not limited by chewing, that no investment in dental tissue is necessary, and that dental wear is not a determinant of senescence as observed in mammals. The absence of age-dependent tooth wear might even be a contributing factor to the slower onset of senescence in birds as compared to mammals. On the other hand, the use of a gizzard requires the intake of suitable grit or stones—an action that represents, in the few studies where this has actually been quantified in birds, a relevant proportion of feeding time (Fritz et al. 2011). Birds have a small intestine that seems very similar to the small intestine of mammals. A duodenum, jejunum and ileum are defined, although these segments are not as histologically distinct as in mammals. The proximal small intestine receives bile from the liver and digestive enzymes from the pancreas, and the absorptive epithelial cells are decorated with essentially the same battery of enzymes and transporters as in mammals. They are short & slightly coiled in meat-eating birds (e.g., raptors) but longer & highly coiled in herbivores (e.g., seed eaters) and omnivores (Figure 29).

Fig 29.Gastrointestinal tracts of a carnivorous hawk, an omnivorous chicken, and 4 herbivorous birds. Note larger size of crop in omnivore and herbivores, and particularly in hoatzin. Ceca are small in hawks and relatively large in grouse. Although ceca are relativelysmall in Hoatzins, Emus, and Ostriches, an expanded foregut (Hoatzins), a much longer midgut (Emus), or a much longer colon (Ostriches) compensates for this (From: Stevens and Hume 1998).

The small intestine is lined with numerous structures called villi (Figure 30). Villi are projections from the intestinal wall that increase the amount of surface area available for absorption. Further increasing the surface area are the numerous microvilli of the cells lining the surface of the villi. Inside each villus are blood vessels that absorb nutrients for transport throughout the body. 11

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

Fig 30.Cross-section of the intestine (ileum) of a Spotted Tinamou (Nothuramaculosa). Villi are lined with columnar epithelium (EP), including goblet cells (arrows) that secrete mucus. The muscle layer includes longitudinal fibers (MI) on the perimeter, circular fibers (Mc), and additional longitudinal fibers at the base of the villi (muscularismuscosae; MM) (From: Chikilian and de Speroni 1996).

The avian large intestine is relatively short. It contains a minimum of non-digestible waste (to help keep birds as light as possible). It also has out-pocketings called caeca. Caeca (Figure 31) are histologically similar to the small and large intestines and found in a wide variety of birds. They are best developed in some waterfowl, gallinaceous birds (like chickens & grouse), and ostriches. In these large ceca, food particles are acted upon

Fig 32.Avian ceca. (A) Little Cormorant, Phalacrocoraxniger,(B) Cattle Egret, Bubulcus ibis, (C) Cotton Teal, Nettapuscoromandelianus, (D) Crested Serpent Eagle, Spilornischeela, (E) Common Quail, Coturnixcoturnix, (F) Indian Ring Dove, Streptopeliadecaocto, (G) Red-wattled Lapwing, Vanellusindicus, (H) Koel, Eudynamysscolopacea, (I) Spotted Owlet, Athenebrama, (J) Indian Roller, Coraciasbenghalensis, (K) Eastern Skylark, Alaudagulgula, & (L) Grey Wagtail,Motacillacaspica (From: Clench 1999).

site for (1) fermentation and further digestion of food (especially for the breakdown of cellulose) and absorption of nutrients, (2) production of antibodies, and (3) the use and absorption of water and nitrogenous components (Clench, 1999). Because birds lack teeth, many ingest pebbles or coarse soil with which to grind food in their gut; some birds tend to consume soil to provide grit (Figure 33). However, Gilardi et al. found that the Peruvian parrots preferred a very fine soil with only a small amount of course material to assist in the assumed grinding function. Most of it is clay which has a very fine particle size, and not suitable for the grinding function.

Fig 31.Avian digestive system. The large intestine consists of a short colon and, typically, a pair of ceca.

bycecal secretions, bacteria, and fungi and nutrients can be absorbed. Some birds (e.g., Passeriformes, Falconiformes, Ciconiiformes, and Pelecaniformes) have very small (Figre 32) ceca called lymphoid ceca. Lymphoid ceca are not important in digestion but contain lymphocytes (white blood cells) that produce antibodies (Clench 1999). At various times and under various conditions, ceca are the

Fig 33.In birds, geophagy (the intentional consumption of soil) is known for geese, parrots, cockatoos, pigeons, cracids, passeriforms, hornbills, &cassuaries.

The cloaca (Figure 34) is an expanded, tubular structure 12

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

that serves as the common opening of the digestive, reproductive and urinary systems, which opens to the outside of the bird as the vent. It is divided into three sections: (1) coprodaeum - receives waste from the large intestine, (2) urodaeum - receives urine from the kidneys (via the ureters) and sperm & eggs from the gonads, and (3)proctodaeum - stores (temporarily) and ejects material; closed posteriorly by the muscular anus.

Fig 34.Avian cloaca. The bursa of Fabricius is located on the dorsal wall. The bursa is most prominent in young birds and serves as the area where B-lymphocytes (the white blood cells that produce antibodies) are generated (T-lymphocytes are generated in the Thymus). Once produced, the Blymphocytes migrate to lymphoid tissue in other parts of the body & the bursa of Fabricius atrophies.

The liver produces bile that is transported to the small intestine via the bile duct. Bile emulsifies fats (or, in other words, breaks fats down into tiny particles). Emulsification is important because it physically breaks down fats into particles than can then be more easily digested by enzymes (lipase produced by intestinal cells and the pancreas). Bile is stored in the

Fig 35.Accessory organsinlucdes the pancreas, liver, and gall bladder. Liver produced bile, which emulsifies fat. Pancreas produces a juice which containts bicarbonate solution that helps neutralize the acids.

gall bladder which is connected to the duodenum through the cystic duct. The bile is concentrated by the removal of water

and is made available to the duodenum when fatty foods stimulate a hormone response to gallbladder to send out the stored bile. The pancreas produces pancreatic juice that is transported to the small intestine. This 'juice' contains a bicarbonate solution that helps neutralize the acids coming into the intestine from the stomach plus a variety of digestive enzymes. The enzymes help break down fats, proteins, and carbohydrates. The pancreas also produces the hormones insulin and glucagon which regulate blood sugar levels(cells (Figure 36) that produce these two hormones make up the 'islets of Langerhans).

Fig 36.Avian pancreas tissue. Cells that produce the two hormones, insuin and glucagon, make up the 'islets of Langerhans.

2.5 RespiratorySystem The avian respiratory system delivers oxygen from the air to the tissues and also removes carbon dioxide. Avian‘s respiratory system plays an important role in thermoregulation which maintains its normal body temperature (Dubach, 1981). Due to the high metabolic rate required for flight, birds have a high oxygen demand (Maina, 1989). The avian respiratory system is different from that of other vertebrates, with birds having relatively small lungs plus nine air sacs that play an important role in respiration (but are not directly involved in the exchange of gases) (Dubach, 1981). The avian respiratory (Figure 37) consist of nostrils, nasal cavity, larynx, trachea, lungs which functions just like the function of these parts on mammalian respiratory system. But for avian respiratory system the larynx does not have vocal chords therefore it is not involved in voice production. Also, the small flap of tissue covering the glottis is not present (Maina, 2008). Birds lack a diaphragm and they have nine airsacs which is the most important part of their respiratory system (Maina, 1989). The nine air sacs (Figure 38) can be divided into anterior sacs (interclavicular, cervicals, & anterior thoracics) & posterior sacs (posterior thoracics& abdominals). Air sacs have very thin walls with few blood vessels (Powell and Hopkins, 2004). The air sacs permit a unidirectional flow of air through the lungs.Unidirectional flow means that air moving through bird lungs is largely 'fresh' air & has a higher oxygen content 13

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

Fig 37.Avian respiratory system.The avian respiratory consist of nostrils, nasal cavity, larynx, trachea, lungs which functions just like the function of these parts on mammalian respiratory system. (From: Sereno et al., 2008)

trachea. Air moves through the trachea to the syrinx, which is located at the point just before the trachea divides in two. It passes through the syrinx and then the air stream is divided in two as the trachea divides. The air does not go directly to the lung, but instead travels to the caudal (posterior) air sacs. A small amount of air will pass through the caudal air sacs to the lung (Reese et al., 2006). During the first expiration (Figure 39B), the air is moved from the posterior air sacs through the ventrobronchi and dorsobronchi into the lungs. The bronchi continue to divide into smaller diameter air capillaries. Blood capillaries flow through the air capillaries and this is where the oxygen and carbon dioxide are exchanged. When the bird inspires the second time, the air moves to the cranial air sacs. On the second expiration, the air moves out of the cranial air sacs, through the syrinx into the trachea, through the larynx, and finally through the nasal cavity and out of the nostrils (Reese et al., 2006).

(O'ConnorandClaessens, 2005).The lungs of birds are less flexible, and relatively small, but they are interconnected with a system of large, thin-walled air sacs in the front (anterior) and back (posterior) portions of the body. These, in turn, are connected with the air spaces in the bones.Evolution has created an ingenious system that passes the air in a one-way, twostage flow through the bird's lungs.

Fig 38.Functionally, these 9 air sacs can be divided into anterior sacs (interclavicular, cervicals, & anterior thoracics) & posterior sacs (posterior thoracics& abdominals). Air sacs have very thin walls with few blood vessels. So, they do not play a direct role in gas exchange. Rather, they act as a 'bellows' to ventilate the lungs (Powell 2000).

Respiration in birds requires two respiratory cycles (inspiration, expiration, inspiration, expiration) to move the air through the entire respiratory system. In mammals, only one respiratory cycle is necessary (Duncker, 1971). During the first inspiration (Figure 39A), the air travels through the nostrils of a bird. From there it passes through the larynx and into the

Fig 39.Schematic representation of the lungs and air sacs of a bird and the pathway of gas flow through the pulmonary system during inspiration and expiration. For purposes of clarity, the neopulmonic lung is not shown. The intrapulmonary bronchus is also known as the mesobronchus.A Inspiration. B – Expiration.

In the avian lung, oxygen diffuses (by simple diffusion) from the air capillaries into the blood & carbon dioxide from the blood into the air capillaries. This exchange is very efficient in birds for a number of reasons. First, the complex arrangement of blood and air capillaries in the avian lung creates a substantial surface area through which gases can diffuse. The surface area available for exchange varies with bird size.A second reason why gas exchange in avian lungs is so efficient is that the blood-gas barrier through which gases 14

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

diffuse is extremely thin. This is important because the amount of gas diffusing across this barrier is inversely proportional to its thickness. Among terrestrial vertebrates, the blood-gas barrier is thinnest in birds. Natural selection has favored thinner blood-gas barriers in birds and mammals because endotherms use oxygen at higher rates than ectotherms like amphibians and reptiles. Among birds, the thickness of the blood-gas barrier varies, with smaller birds generally having thinner blood-gas barriers than larger birds (West, 2009) Also contributing to the efficiency of gas exchange in avian lungs is a process called cross-current exchange. Air passing through air capillaries and blood moving through blood capillaries generally travel at right angles to each other in what is called cross-current flow (Figure 40; Makanya and Djonov 2009). As a result, oxygen diffuses from the air capillaries into the blood at many points along the length of the parabronchi, resulting in a greater concentration of oxygen (i.e., higher partial pressures) in the blood leaving the lungs than is possible in the alveolar lungs of mammals.

Fig 40.Diagram of parabronchial anatomy, gas-exchange region of the bird's lung-air-sac respiratory system. The few hundred to thousand parabronchi, one of which is fully shown here, are packed tightly into a hexagonal array. The central parabronchial lumen, through which gas flows unidirectionally during both inspiration and expiration is surrounded by gas-exchange tissue composed of an intertwined network of blood and air capillaries. On the left side of this diagram, the lumen of the parabronchus leads into multiple chambers called atria (A) that, in turn, lead into smaller chambers called infundibulae (I). Branching from the infundibulae are numerous air capillaries. On the right side of this diagram are the blood vessels. Arteries (a) lead into the capillaries that are closely associated with the air capillaries. It is here (air and blood capillaries) where oxygen and carbon dioxide are exchanged. After flowing through the capillaries, blood then moves into the veins (v) that will take the blood out of the lungs (From: Duncker 1971 as reprinted in Powell 2000).

Contrary to what was once believed, the rhythm of a bird's respiratory two-cycle pump is not related to the beats of its wings. Flight movements and respiratory movements are independent. The heart does the pumping required to get oxy-

genated blood to the tissues and to carry deoxygenated blood (loaded with carbon dioxide) away from them. Because of theefficiency of the bird's breathing apparatus, the ratio of breaths to heartbeats can be quite low. A mammal takes about one breath for every four and one-half heartbeats (independent of the size of the mammal), a bird about one every six to ten heartbeats (depending on the size of the bird).

2.6 Circulatory System Birds have very efficient cardiovascular systems that permit them to meet the metabolic demands of flight (and running, swimming, or diving). The cardiovascular system not only delivers oxygen to body cells (and removes metabolic wastes) but also plays an important role in maintaining a bird's body temperature. Birds have very efficient cardiovascular systems that permit them to meet the metabolic demands of flight (and running, swimming, or diving). The cardiovascular system not only delivers oxygen to body cells (and removes metabolic wastes) but also plays an important role in maintaining a bird's body temperature. Birds tend to have larger hearts (Figure 41) than mammals (relative to body size and mass), and of the same basic design as that of a mammal. It is a four-chambered structure of two pumps operating side by side. One two-chambered pump receives oxygen-rich blood from the lungs and pumps it out to the waiting tissues. The other pump receives oxygen-poor blood from the tissues and pumps it into the lungs. This seg-

Fig 41.Dorsoventral (A) and lateral (B) thoracic radiographs from a grey heron, showing the normal avian cardiac silhouettes, which are located nearly along the longitudinal axis of the body (Machida and Aohagi 2001).

regation of the two kinds of blood (which does not occur completely in reptiles, amphibians, and fishes) makes a bird's circulatory system, like its respiratory system, well equipped to handle the rigors of flight. Because the left ventricle must generate greater pressure to pump blood throughout the body (in contrast to the right ventricle that pumps blood to the lungs), the walls of the left ventricle are much thicker & more muscular. Avian hearts also tend to pump more blood per unit time than mammalian hearts. In other words, cardiac output (amount of blood pumped per minute) for birds is typically greater than that for mammals of the same body mass. Cardiac output is influenced by both heart rate (beats per minute) and stroke volume (blood pumped with each beat). 'Active' birds 15

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increase cardiac output primarily by increasing heart rate. In a pigeon, for example(Butler et al. 1977): Rest Heart rate 115 beats/min Stroke volume 1.7 ml Cardiac output 195.5 ml/min Oxygen consumed 20.3 ml/min

Active Increase 670 beats/min 5.8x 1.59 ml 0.9x 1065 ml/min 5.4x 200 ml/min 10x

In general, bird hearts 'beat' at somewhat lower rates than mammals of the same size but pump more blood per 'beat‘. Blood pumped by the avian heart enters the blood vessels. The main types are: (a) arteries - carry blood away from the heart & toward the body cells; (b) arterioles - 'distribute' blood (that is, direct blood where needed with more going to active tissues & organs & less to less active tissues & organs) by vasodilating&vasoconstricting; (c)capillaries - exchange of nutrients, gases, & waste products between the blood & the body cells; (d) venules (small veins) & veins- conduct blood back to the heart.

veins drain the pectoral muscles and anterior thorax; (e) the superior vena cavae (or precavae) drain the anterior regions of the body; (f) the inferior vena cava (or postcava) drains the posterior portion of the body; (g) the hepatic vein drains the liver; (h) the hepatic portal vein drains the digestive system; (i) the coccygeomesenteric vein drains the posterior digestive system & empties in the hepatic portal vein; (j) the femoral veins drain the legs; (k) the sciatic veins drain the hip or thigh regions; (l)the renal & renal portal veins drain the kidneys. The avian blood is consists of plasma + formed elements. The plasma is largely water (~85%) plus lots of protein (~911%); other constituents of blood include glucose (blood glucose levels in birds are greater than in mammals; about 200400 mg/dl), amino acids, waste products, hormones, antibodies, & electrolytes. The formed elements include red blood cells (or erythrocytes), white blood cells (or leucocytes), and thrombocytes. bird red blood cells are elliptical in shape and nucleated. In most species, red blood cells are about 6 x 12 microns in size (mammalian RBC's are typically 5.5 - 7.5 microns in diameter). Typical concentrations are 2.5 to 4 million/cubic mm. Avian red blood cells have a lifespan of 28-45 days (shorter than mammals, e.g., about 120 days in humans). Red blood cells contain hemoglobin, the molecule responsible for transporting oxygen throughout the body, and are produced in the bone marrow. However, many bird bones are pneumatic (penetrated by air sacs) and do not contain marrow. Hemopoietic bone marrow (red-blood-cell-producing marrow) is located in the radius, ulna, femur, tibiotarsus, scapula, furcula (clavicles), pubis,and caudal vertebrae.Bird thrombocytes (shown above with two red blood cells), also nucleated, are comparable to the non-nucleated platelets of mammalian blood. Thrombocytes are important in hemostasis (blood clotting). White blood cells play an important role in protecting birds from infectious agents such as viruses and bacteria. Birds have several types of white blood cells (Figure 43).

Fig 42.Avian circulatory system ventral view (left) and dorsal view (right).

Some of the major arteries in the avian circulatory system are (Figure 42): (a) carotids deliver blood to the head (& brain); (b) brachials take blood to the wings; (c) pectorals deliver blood to the flight muscles (pectoralis); (d) the systemic arch is also called the aorta & delivers blood to all areas of the body except the lungs; (e) the pulmonary arteries deliver blood to the lungs; (f) the celiac (or coeliac) is the first major branch of the descending aorta & delivers blood to organs & tissues in the upper abdominal area; (g) renal arteries deliver blood to the kidneys; (h) femorals deliver blood to the legs & the caudal artery takes blood to the tail; (i) the posterior mesenteric delivers blood to many organs & tissues in the lower abdominal area. Some major veins in the avian circulatory system (Figure 42) are: (a) the jugular anastomosis allows blood to flow from right to left side when the birds head is turned & one of the jugulars constricted; (b) the jugular veins drain the head and neck; (c) the brachial veins drain the wings; (d) the pectoral

A

B

C

D

Fig 43. White blood cells present in avian blood. (A) lymphocyte; (B) heterophil; (C) monocytes; and (D) eosinophils.

The lymphocyte (A) is the most numerous white blood cell. Lymphocytes are either T-lymphocytes (formed in the thymus) or B-lymphocytes (formed in the bursa of Fabricius). Blymphocytes produce antibodies; T-lymphocytes attack infected or abnormal cells.The (B) heterophil is the second most numerous WBC in most birds. Heterophils are phagocytic and 16

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

use their enzyme-containing granules to lyse ingested materials. Heterophils are motile and can leave blood vessels to engulf foreign materials.Monocytes (C) are motile cells that can migrate using ameboid movements. Monocytes are also phagocytic.Eosinophils (D) make up about 2 to 3 % of the WBC population of healthy birds. The function of these cells is unclear. The avian cardiovascular system is able to quickly respond to changes in levels of activity (e.g., resting vs. flying) via changes in heart rate, cardiac output, & blood flow (by vasocontriction and vasodilation of vessels). Many birds forage by diving underwater. So, what happens when a bird doesn't have access to air (oxygen)? The quintessential avian diver is the Emperor Penguin, which can attain depths greater than 500 meters while staying submerged for about 12 minutes. In shallower dives, an Emperor Penguin may stay submerged even longer, over 20 minutes. One 'solution' to the oxygen problem is that birds, like penguins,that spend lots of time underwater, store lots of oxygen in their muscles. The muscles of some diving birds contain lots of myoglobin. Myoglobin binds oxygen just like hemoglobin but actually has a higher affinity for oxygen than does hemoglobin. This means that when blood passes through muscle, lots of oxygen is transferred from the blood to the muscle. The chart below illustrates this. In Emperor Penguins, nearly half (47%) of all oxygen in the body is in the muscles. As a result, when a penguin dives, muscle cells have access to lots of oxygen that allows them to remain active. Other tissues, of course, don't 'store' oxygen like muscle. Those tissues, such as the brain, still depend on oxygen being transported in the blood. However, because the skeletal muscles need less oxygen, more is available for other tissues like the brain.When a bird dives, special receptors in the body detect an increase in levels of carbon dioxide (because the bird has stopped breathing). These receptors then stimulate the brain which, in turn, sends nervous impulses that reduce heart rate & cause blood vessels in different parts of the body to either vasoconstrict or vasodilate.

2.7 Muscular System The muscles of birds have also been modified by natural selection to meet the demands of flight. Like their skeletial system, there are also reductions in some muscels to minimize theri weight. Jaw muscles are reduced in many birds (powerful muscles often unnecessary because food is swallowed whole or in large pieces, e.g., owls).Hindlimb muscles are reduced in many species. A bird has some 175 different muscles controlling the movements of its wings, legs, feet, tongue, eyes, ears, neck, lungs, sound-producing organs, body wall and skin. Collectively, the muscles are concentrated near the bird's center of gravity. Largest of all the muscles are the breast muscles, or pectorals. The bird's most massive muscles power flight. Muscles located on each side of the breastbone keel extend outward. These muscles form the bulk of the fleshy mass in the breast and constitute about 15 to 20 percent of the bird's total body weight. Birds power flight primarily by large pectoralis(Figure 44) muscles that depress the wings at the shoul-

Fig 44. The largest muscles in the bird are the pectorals, or the breast muscles, which control the wings and make up about 8 - 11% (Roberts et al., 1997; George and Berger, 1966) of a flighted bird’s body weight. They provide the powerful wing stroke essential for flight (From L. Shyamal).

der. The dominant role and large size of the pectoralis muscle, therefore, enable a critical assessment of how muscle function is tailored to meet the mechanical power requirements of flapping flight over a range of flight conditions.The smaller supracoracoideus muscle of birds, about one-fifth the size of the pectoralis, is the primary wing elevator active during upstroke, particularly at slow to moderate speeds and during hovering (at faster flight speeds, wing elevation is probably produced passively by aerodynamic forces acting on the wings, which remain extended during upstroke to maintain lift through bound circulation (Rayner, 1988; Tobalske et al., 2003). The pectoralis is a large muscle (approx. 8–11% body mass; (Roberts et al., 1997; George and Berger, 1966) that attaches to the humerus of the wing at the deltopectoral crest (Figure 45). In addition to producing mechanical work during downstroke, the pectoralis also pronates the wing. The muscles which furnish the propelling force of the wings are those of the breast, the pectoralis major and the pectoralis minor. The pectoralis major is large, triangular muscle forming the principal part of the bulk of the breast. It arises from the ribs, from the outer portion of the ventral surface of the sternum, from the side of the keel of the sternum, from the furculum and the membrane connecting the furculum with the sternum and the coracoid. The fibers converge, the outer turning under the inner and inserted by a tendon on the greater tuberosity of the humerus. In action,this muscle depresses the wing and thus furnishse the great motive power of flight. The pectoralis minor is much smaller than preceding, and beneath it; arising from the middle portion of the sternum and the membrane attaching the furculum to the sternum and the coracoid. Its fibers converging terminate in a tendon which, after passing through the end of the coracoid, inserted on the inner side of the greater tuberosity of the humerus. This muscle, together with resisting force of the air, elevates the wing after it has been depressed. The smaller supracoracoideus lies deep to the pectoralis, also originating from the keel of the sternum, and is about onefifth of the pectoralis in mass (approx. 2% body mass). By means of its tendon, which inserts and acts dorsally at theshoulder as a pulley, the supracoracoideus elevates (Figure 46, 17

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

Vasquez, 1995;Warrick and Dial, 1998; Hedrick et al., 2007) and, thus, may indirectly affect flight power requirements. However, because of their small size, the intrinsic muscles of the wing probably contribute little additional mechanical power for flight (Biewener, 2011).

Fig 45. (a) Anatomical organization of avian wing musculature (adapted from Dial, 1992, showing key muscles that have been studied, and (b) showing the general sites used to record pectoralis force via deltopectoral crest (DPC) bone strain, pectoralis fascicle strain and neuromuscular activation (EMG).

47) and supinates the wing during upstroke (Poore et al., 1997; Kaplan and Goslow, 1989; Rosser and George, 1986).

Fig 47.Downstoke and upstroke of flight muscles. (a) On the downstroke, the pectoralis pulls tight, pullin the wing down. (b) On the upstroke, the supracoracoideus pulls a tendon that loops around the foramen triosseum; this pulls the wing bone.

The pectoralis muscle powers the downstroke(Figure 47) and is proportionately very large in birds (up to 35% of body weight). The supracoracoideus is much smaller and has a tendon which curves around to attach to the top of the humerus. The supracoracoideus can provide power to the upstroke if required but more usually produces a rapid rotation of the humerus at the top of the upstroke (Poore et al, 1997). Fig 46.Flight muscles. Pectoralis or downstroke muscle originates on the keel and inserts on the underside of the humerus. Supracoracoideus or upstroke muscle originates on the keel and inserts on the upper side of the humerus. The massive pectoralis muscle pushes the wing downward in flight and supports the bird while soaring. The opposing supracoracoideus muscle raises the wing in flight.

Smaller extrinsic and intrinsic wing muscles assist in modulating wing orientation and controlling wing shape. These muscles probably contribute to adjustments of the wing's performance as an aerofoil (Dial, 1992; Dial and Gatesy, 1993;

2.8 Urogenital System In anatomy, the urogenital system is the organ system of the reproductive organs and the urinary system. 2.8.1 Urinary System The urinary system is the body‘s waste removal system. The kidneys' main function is to process and remove wastes (created from cell metabolism) and excess ions from the blood, regulate blood volume and maintain electrolyte balance. Osmoregulation refers to the various mechanisms by which 18

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

products of metabolism and ions, that are voided in the urine. Kidneys also play an important role in conserving water and reabsorbing needed substances (like glucose). The urinary organs of birds consist of paired kidneys and the ureters (Figure 48), which transport urine to the urodeum of the cloaca. Avian kidneys are divided into units called lobules. Each lobule has a cortex (outer area) and medulla (or medullary cone; Figure 49). In terms of volume, the avian kidney is primarily cortex (71-81%), plus a relatively small medulla (range 5-15%) & blood vessels larger than capillaries (range 10-13%). The functional unit of the kidney is the nephron. Avian kidneys have two kinds of nephrons. A reptilian-type, with no loops of Henle are located in the cortex, and a mammaliantype with long or intermediate length loops, are located in the medulla (Figure 50). In birds, only a small percentage of nephrons (15-25%) contain a loop of Henle (i.e., looped nephrons). Nephrons filter the blood plasma to eliminate waste products, but, in doing so, must not lose needed materials (like glucose) or too much water. Blood enters nephrons via small arteries called afferent arterioles (Figure 51). This blood enters the glomerulus (a collection of capillaries; Figure 52) under high pressure and 'filters' through the walls of the capillaries and the walls of a surrounding structure called a capsule. The filtrate that moves from the glomerular capsule into the proximaltubules is basically plasma without protein (the protein Fig 48. Urine is carried from the avian kidneys to the cloaca (and, specifically, the top section called the coprodeum) by the ureters (male testes and vas deferens are also illustrated, showing the change is size between the breeding and non breeding seasons).

birds regulate water and electrolyte levels in their bodies. Body fluids, most importantly extracellular osmolality and blood volume, are regulated within narrow limits. The ‗osmo-‗ in osmoregulation refers to osmosis, the process by which water passes through semipermeable membranes (like cell membranes) in response to differences in solute concentrations. Of course, living cells can only survive if the concentrations of solutes, or electrolytes, remain very similar inside (intracellular fluid) and outside (extracellular fluid) of cells. Insuring that this is the case requires that both water and electrolyte levels in the body be regulated very precisely. In mammals, the kidneys play the critical role in this process. In birds, on the other hand, the kidneys, lower intestine, and, in some species, salt glands all play important roles in osmoregulation.Water balance requires the input matches output. Most birds can obtain water directly by drinking. Birds can also obtain water via the foods they ingest. For example, carnivores ingest animal tissue that is primarily water, frugivores consume fruits containing water, and the nectar consumed by nectarivores is, of course, largely water.Even foods that seemingly contain little water can serve as a water source because water is produced as a byproduct of cellular metabolism. This metabolic water can be of particular importance to birds in arid environments (Williams, 1996). The role of bird kidneys, like the kidneys of other vertebrates is filtration, excretion or secretion, and absorption. They filter water and some substances from blood, such as waste

Fig 49.Lobule of an avian kidney. The medullary cones include the loops of Henle and collecting ducts of nephrons plus a number of capillaries called the vasa recta. The avian renal medulla is cone shaped because the number of loops of Henle decreases toward the apex of the medullary cones.

molecules are too large). That filtrate, therefore, contains lots of important substances. In the proximal convoluted tubules, those needed substances such as vitamins and glucose are reabsorbed into the the blood (Figure 7). Even sunbirds, with a diet rich in glucose, are able to reabsorb almost all (98%) of the 19

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

more of a hormone called arginine vasotocin (AVT) into the blood. In the kidneys, AVT causes a reduction in the glomerular filtration rate (the rate at which plasma filters from the glomeruli into the glomerular capsule) so less water moves from the blood into the kidney tubules. In addition, AVT increases the permeability of the walls of collected ducts to water by opening protein water channels called aquaporins. As the collecting ducts become more permeable, more water moves by osmosis out of the collecting ducts (because of the higher solute concentration in the medullary cones) and can be reabsorbed by kidney capillaries. Studies to date suggest that the extent to which AVT can reduce urine production (and water loss) varies among species, but, in general, AVT is less

Fig 50.Avian nephrons. Most avian nephrons (75-85%) are 'reptilian type', with no loops of Henle. Only 15-25% are 'mammalian type' that have loops of Henle.

glucose that filters into the kidney tubules (McWhorter et al., 2004). Other than mammals, birds are the only vertebrates that conserve body water by producing urine osmotically more concentrated than the plasma from which it is derived. However, the ability of birds to concentrate urine is limited compared to mammals.This reduced capacity of avian kidneys to concentrate urine (compared to mammals) means that more water accompanies the solutes that travel from the kidneys

Fig 51. Nephron components (mammalian type nephron shown):1 = glomerular capsule, 2 = glomerulus, 3 = afferent arteriole, 4 = efferent arteriole, 5 = proximal convoluted tbule, 6 = distal convoluted tubule, 7 = collecting duct, 8 = loop of Henle, &9 = peritubular capillaries (or vasa recta).Plasma is filtered from the glomerular capillaries into the glomerular capsule. Filtrate then travels through the tubules and loop of Henle before entering the collecting duct.

through ureters to the cloaca. Water-deprived birds do have a mechanism for reducing the amount of water leaving the kidneys. In response to dehydration, the pituitary gland releases

Fig 52.Glomeruli of an Anna's Hummingbird. In some caes (A), the glomerular capillary is twistedinto a spiral (scale bar = 17 micrometers), but more typically (B) is bent into one or twoloops that fold back on themselves (scale bar = 20 micrometers). (From: Beuchat et al., 1999).

effective in conserving water than the mammalian equivalent (antidiuretic hormone, or ADH; Nishimura and Fan 2003). Therefore, water-deprived birds tend to produce more urine, and lose more water from the kidneys, than would a similarsized water-deprived mammal. An important part of the diet of all birds is protein. Proteins are composed of subunits called amino acids, and those amino acids are sometimes used as a source of energy or are converted into fats or carbohydrates. When amino acids are used for energy or converted to fats or carbohydrates, the amine (NH2) group must be removed. These amine groups are toxic and must be eliminated. Some organisms excrete these nitrogenous wastes as ammonia (e.g., aquatic animals like bony fishes and amphibians) or urea (e.g., terrestrial amphibians and mammals). Birds (and reptiles) excrete these wastes primarily as uric acid. Although excreting nitrogenous wastes as uric acid has its advantages (e.g., not very toxic, not soluble in water so it can be excreted without using lots of water, and it can be stored in eggs without damaging embryos), uric acid is a more complex molecule than either ammonia or urea and synthesizing it requires more energy. Once in the cloaca, both urine and the uric acid particles are sent to the large intestine where microorganisms recover the protein coat of the uric acid particle and water and electrolytes in the urine can be reabsorbed and balanced. Any free amino acids and sugars are taken up by specific transporters from the large intestines. The rest is than sent back into the cloaca. Uric 20

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

acid functions as a magnet to pick off free radicals. Studies have shown that reduction of uric acid in chickens increases the rate of tissue aging to a rate found in human diabetics.

2.8.2 Reproductive System Male organs exhibit all the essential characteristics of the oviparous type of structure. Male birds have a pair of testes that resemble a bean shape and each are located in front of the top lobe of the kidneys.The testes are situated high up in the abdomen, whence they never descend into an external scrotum. They are two (Figure 53a); in form more or less oval, situated near the upper extremities of the kidneys. They vary remarkably in color in different birds (Owens, 1866). The periodical variations of size which the testicles undergo are very remarkable; and the limited period during the frequency and energy with which it is exercised. During non-breeding season the testes are difficult to locate due to their small size, but during breeding season they may grow as much as several hundred times their non-breeding size. The proportional size which the testes acquire (Figure 53) at the breeding season is immense. It rarely happens that both testes are developed in exactly the same degree: the left is commonly the largest; but sometimes the right exceeds the left (Owens, 1866). A

B

Fig 53.(A)a – testes, b – remanant of the primordial kidney, c – vas deferens. (B)Testes of the House-Sparrow which commences with the glands as they appear in January, when they are no bigger than pins’ head, and ends with their full development in April.

As in mammals, the sperm cells of birds cannot develop fully at high temperatures that are found within the body cavity. Some birds experience a nightly drop in body temperature that allows the sperm cells to develop, while other birds have a swelling at the end of the tube (vas deferens). This tube connects the testes to the cloaca, and functions like a mammals scrotum holding the sperm away from the higher body temperatures that are within the abdomen. The female organs consist of the ovary and the oviduct that leads to the cloaca. With most bird species, the ovary is on the left side with the right side being underdeveloped and non

Fig 54.Avian female reproductive system.In most birds, only the left ovary and oviduct persist. The ovary enlarges greatly during the breeding season. Active ovaries resemble bunches of tiny grapes -- the developing follicles. The oviduct opens medially to it in a funnel-shaped ostium. Ovulation results in the release of an egg from a mature follicle on the surface of the ovary. The egg, with extensive food reserves in the form of concentric layers of yolk, is picked up by the ostium and ciliary currents carry it into the magnum region. Over about three hours the egg receives a coating of albumen.The egg then passes into the isthmus, where the shell membranes are deposited. This takes about one hour. The egg them moves to the uterus, or shell gland, where the calcareous shell is added and, in some birds, pigment is added in characteristic patterns. The egg then passes into the vagina and cloaca for laying.

functional. It is thought that being only one sided reduces body weight and eliminates the possibility of carry two large, fragile eggs in the abdomen cavity at the same time. The ovary when mature looks like a cluster of grapes. It may contain up to 4,000 small ova that can develop into yolks. Yolk protein, lipids and fats are manufactured in the liver and travel through the bloodstream to the immature ovum, during the maturation stage. Each yolk is attached to the ovary by a thin membrane sac or follicle having a fine network of blood vessels. The germinal disc of a developing yolk contains the single ovum cell which, after fertilization develops into a chick. The ovary enlarges during breeding season as much as fifty times its non-breeding weight. Most bird species rub their cloacal areas together to transfer the male's sperm but ostriches, rheas, strokes, flamingos, ducks and a few other families actually have an erectile grooved penis on the back wall of the cloaca to transfer sperm. Near the junction of the vagina and shell gland of female birds are deep glands lined with simple columnar epithelium. These are the sperm storage tubules, so called because they can store sperm for long periods of time (10 days to 2 weeks). After an egg is laid, some of these sperm may move out of the tubules into the lumen of the tract, then migrate farther up to 21

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

fertilize another egg. Birds' eggs, like the birds themselves, vary enormously in size. The largest egg from a living bird belongs to the ostrich. It is over 2000 times larger than the smallest egg produced by a hummingbird. Ostrich eggs are about 180 mm long and 140 mm wide and weigh 1.2 kg. Hummingbird eggs are 13 mm long and 8 mm wide and they weigh only half of a gram.

2.9 Endocrine System The Endocrine system consists of various glands and nodes which secrete hormones. Hormones are chemical messengers which travel in the blood to activate target cells. These target cells have special receptors, into which only certain hormones can fit. For example, testosterone act on the male gonads, but not the adrenal glands (Hartenstein, 2006). Avian endocrine system is composed of pituitary, hypothalamus, pineal body, adrenal glands, thyroid, parathyroid, ultimobrachial bodies, islets of Langerhans and gonads (Colombo et al., 2006). 2.10 Nervous System The avian nervous system consists of the Central Nervous System which consists of the brain and spinal cord, and the Peripheral Nervous System which includes the cranial and spinal nerves, autonomic nerves and ganglia, and sense organs.

Fig 55.Gross anatomy of the avian brain. (A) Left lateral and (B) caudaldorsal views of the brain ofColumba livia.(C)Anser sp. in ventral view. (Modified after Portmann & Stingelin, 1961.) (D–G) Variability of wulst position anddevelopment illustrated through dorsal views of prepared skulls revealing alcohol-fixed brains of (D)Larus canus(rostralposition),(E)Larusargentatus(rostral-central position), (F)Anassp. (caudalposition)and(G)Sturnus vulgaris(wulst occupying most of dorsal telencephalon).

The avian brain shares many features with the brains of living reptiles (Jerison, 1973). The forebrain is largely involved in higher-level processing of sensory information, cognition, and

memory. Traditionally the forebrain is divided into two main structural regions, the telencephalon and the diencephalon (Walsh and Milner, 2011). At the cellular level, the avian telencephalon is composed of stacked layers of differentiated cells (Reiner et al., 2004). The hippocampus is situated in a caudal position on the telencephalon and is implicated in memory functions and spatial awareness, including navigation (Gagliardo et al., 1999; Streidter, 2005). Paired olfactory bulbs (olfactory lobes) are normally visible at the rostral extremity of the telencephalon. The relative size of these structures is variable within bird species, but in all cases the lobes represent a far smaller proportion of the overall brain size than they do in reptiles, particularly in crocodiles and alligators (Pearson, 1972). Only the pineal and the pituitary (hypophysis) glands of the diencephalon are easily observable. The pineal is normally relatively small and visible on the dorsocaudal surface of the brain between the rostralmost extent of the cerebellum and the caudalmost margins of the telencephalic hemispheres. The pituitary is a rounded structure of variable form (Wingstrand, 1951) that projects ventrally from between the caudal region of the optic chiasma and rostral region of the rhombencephalon. The mid-brain (mesencephalon) of birds is broadly like that of most vertebrates in that it is composed of a tegmentum (primarily concerned with general motor- and ocularmotor control) and a tectum (further separated into the optic tectum and torus semicircularis involved in visual and auditory stimuli integration and routing to the diencephalon)(Dubbledam, 1998). The occulomotor nerve (CN III) originates in this region, projecting rostrally into the orbit. The origin of the trochlear nerve (CN IV) is approximately in the ventrolateral region of the mesencephalon. The hindbrain (rhombencephalon) is composed primarily of the cerebellum and medulla, and is mostly involved in motor control (Walsh and Milner, 2011). The avian cerebellum possesses a distinct flocculus, which projects from its lateral walls through the arch of the anterior semicircular canal of the inner ear labyrinth (Larsel, 1967). The avian rhombencephalon (medulla) is an elongate structure situated ventral to the cerebellum. It grades caudally into the spinal chord (Pearson, 1972). Seven cranial nerves (numbered caudally from CN V to XII) exit the rhombencephalon along the lateral and ventral surfaces. The trigeminal (CN V) normally splits into two branches close to its origin on the lateral surface of the medulla. CN V1 extends rostrally to relay sensory impulses from the eye, while the second branch subdivides into the maxilliary CN V2 and mandibularCNV3 that conduct mechanoreceptor information, particularly from the beak. Since object manipulation is mainly achieved using the beak in nearly all bird species, this nerve in birds is large. Cranial nerve VI, the abducens, exits the medulla ventrally and carries motor impulses to the lateral rectus and bulbar retractor muscles of the eye. The facial nerve (CN VII) serves both motor and sensory functions, including gustatory information (Gentle& Clarke, 1985). Birds possess virtually no facial musculature, and correspondingly the avian CN VII is more poorly developed than in 22

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013

mammals. The vestibulocochlear nerve (CN VIII) is involved in only sensory functions, conducting auditory signals from the cochlear duct, and vestibular information from the saccule and semicircular canals. Cranial nerve IX (glossopharyngeal) relays sensory (particularly taste) and motor impulses, and generally exits the lateral surface of the medulla with the vagus nerve. The vagus itself (CN X) performs central roles in conducting sensory and motor impulses that regulate autonomic functions, principally in the heart, digestive tract, and lungs. The accessory nerve (CN XI) forms a further branch off the main CN IX/X branch, and conveys mainly motor impulses to muscles of the neck. The hypoglossal nerve (CN XII) is the final cranial nerve, carrying mostly motor impulses to the tongue and throat (Milner and Walsh, 2009).

[12] [13] [14]

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4 SUMMARY Unlike any other vertebrates, avians have the power of flight. Birds show a marvelous diversity not only of species but of flight adaptations. Presence of feathers separates birds from all other living vertebrates. Feathers are associated with flight - the major characteristic feature of birds is the capacity for flight. Birds‘ overall anatomy and physiology are adapted to the demands of flight. Their structure combines strength and lightweight. (a) Fusion and elimination of some bones and pneumatization of the avian skeleton, (b) powerfull and lightweight flight muscles, (c) very efficient respiratory system (compared to mammals), and a (d) powerful and large heart (compared to mammals) are the anatomical traits of the aves.

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REFERENCES [1]

Biewener A. A. 2011. Muscle function in avian flight: achieving power and control. [2] Bonser, B. H. C. 1996. Comparative mechanics of bill, claw and feather keratin in the Common Starling Sturnus vulgaris. Journal of Avian Biology 27: 175-177. [3] Butler, P. J. 2001. Diving beyond the limits. News in Physiological Sciences 16: 222-227. [4] Butler, P. J., N. H. West, and D. R. Jones. 1977. Respiratory and cardiovascular responses of the pigeon to sustained, level flight in a wind tunnel. Journal of Experimental Biology 71:7-26 [5] Davie, Oliver. 1900. Methods in the art of taxidermy. Philadelphia: David McKay [6] Dial K. P. 1992. Activity patterns of the wing muscles of the pigeon (Columba livia) during different modes of flight. J. Exp. Zool. 262, 357–373. (doi:10.1002/jez.1402620402) CrossRefWeb of Science [7] Dial K. P., Gatesy S. M. 1993. Neuromuscular control and kinematics of the wings and tail during maneuvering flight. Am. Zool. 33, 5. [8] Dubach, M. 1981. Quantitative analysis of the respiratory system of the House Sparrow, Budgerigar, and Violet-eared Hummingbird. Respiration Physiology 46: 43-60. [9] Duezler Ayhan, Ozgel Ozcan, Dursun Nejdet (2006). "Morphometric Analysis of the Sternum in Avian Species". Turk. J. Vet. Anim. Sci. 30: 311–314. [10] Duncker, H.-R. 1971. The lung air sac system of birds. Advances in Anatomy, Embryology, and Cell Biology 45: 1–171. [11] Elias, P. M., and G. K. Menon. 1991. Structural and biochemical corre-

[21] [22] [23]

[24]

[25]

[26]

[27]

[28]

[29]

lates of the epidermal permeability barrier. Advances in Lipid Research 24:1-26. Gill, Frank B. (2007). Ornithology. New York: W. H. Freeman and Company. pp. 134–136. ISBN 0-7167-4983-1. Glen, C. L., and M. B. Bennett. 2007. Foraging modes of Mesozoic birds and non-avian theropods. Current Biology 17: R911-R912. Gregory, R. D., Noble, D., Field, R., Marchant, J. H., Raven, M. and Gibbons, D. W. 2003. Using birds as indicators of biodiversity.Ornis Hungaria 12–13: 11–24. Gregory, R. D., van Strien, A. J., Vorisek, P., Gmelig Meyling, A. W., Noble, D. G., Foppen, R. P. B. and Gibbons, D. W. 2005. Developing indicators for European birds. Phil. Trans. R. Soc. Lond. B. 360: 269– 288 Hartenstein, V.2006. "The neuroendocrine system of invertebrates: a developmental and evolutionary perspective". The Journal of endocrinology 190 (3): 555Colombo, L; Dalla Valle, L; Fiore, C; Armanini, D; Belvedere, P (2006 Apr). "Aldosterone and the conquest of land". Journal of endocrinological investigation 29 (4): 373–9. Hedrick T. L., Usherwood J. R., Biewener A. A. 2007. Low speed maneuvering flight of the rose-breasted cockatoo (Eolophus roseicapillus). II: Inertial and aerodynamic reorientation. J. Exp. Biol. 210, 1912–1924. Homberger, D. G., and A. H. Brush. 1986. Functional morphology and biochemical correlations of the keratinized structures of the African Gray Parrot, Psittacus erithacus (Aves). Zoomorphology 106: 103114. Kaplan S. R., Goslow G. E. Jr. 1989. Neuromuscular organization of the pectoralis (pars thoracicus) of the pigeon (Columba livia): implications for motor control. Anat. Rec. 224, 426–430. Kaplan, S. R., Goslow, G. E. Jr. 1989. Neuromuscular organization of the pectoralis (pars thoracicus) of the pigeon (Columba livia): implications for motor control. Anat. Rec. 224, 426–430. Lennerstedt, I. 1975a.. Pattern of pads and folds in the foot of European Oscines (Aves, Passeriformes). Zool. Scr, 4101-109. Lucas, A. M. 1970. Avian functional anatomic problems. Fed. Proc. 29:1641-1648. Maina, J. N. 2008. Functional morphology of the avian respiratory system, the lung-air system: efficiency built on complexity. Ostrich 79: 117-132. Maina, J.N. 1989. The morphometry of the avian lung. Pp. 307-368 in Form and function in birds (A.S. King and J. McLelland, eds.). Academic Press, London. Menon, G. K. 1984. Glandular functions of avian integument: an overview. Journal of the Yamashina Institute for Ornithology 16:1– 12. Menon, G. K., P. F. A. Maderson, R. C. Drewes, L. F. Baptista, L. F. Price, and P. M. Elias. 1996. Ultrastructural organization of avian stratum corneum lipids as the basis for facultative cutaneous waterproofing. Journal of Morphology 227:1-13. Negro, J. J., J. H. Sarasola, F. Fariñs, and I. Zorrilla. 2006. Function and occurrence of facial flushing in birds. Comparative Biochemistry and Physiology A 143: 78-84. O'Connor, P. M. and L. P. Claessens. 2005. Basic avian pulmonary design and flow-through ventilation in non-avian theropod dinosaurs. Nature 436:253-256. Paul, Gregory S. 2002. "Looking for the True Bird Ancestor". Dinosaurs of the Air: The Evolution and Loss of Flight in Dinosaurs and Birds. Baltimore: Johns Hopkins University Press. pp. 171–224. 23

Mindanao State University – General Santos City, College of Natural Science and Mathematics Department of Biology, October-2013 [30] Pelletier, D., M. Guillemette, J.-M. Grandbois, and P. J. Butler. 2007. It is time to move: linking flight and foraging behaviour in a diving bird. Biology Letters 3: 357-359. [31] Poore S. O., Ashcroft A., Sanchez-Haiman A., Goslow G. E. Jr. 1997. The contractile properties of the m. supracoracoideus in the pigeon and starling: a case for long-axis rotation of the humerus. J. Exp. Biol. 200, 2987–3002. [32] Poore S. O., Sanchez-Haiman A., Goslow G. E. J. 1997. Wing upstroke and the evolution of flapping flight. Nature 387, 799–802. (doi:10.1038/42930) CrossRef [33] Powell, F. L. and S. R. Hopkins. 2004. Comparative physiology of lung complexity: implications for gas exchange. News in Physiological Science 19:55-60. [34] Proctor, Noble S.; Lynch, Patrick J. (October 1998). Manual of Ornithology: Avian Structure and Function. Yale University Press. p. 214. ISBN 0-300-07619-3. [35] Prum R.O. 2008. "Who's Your Daddy". Science 322 (5909): 1799–1800. doi:10.1126/science.1168808. PMID 19095929. [36] Prum, R. O., and R. Torres. 2003. Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays. Journal of Experimental Biology 206: 2409-2429. [37] Raikow R. 1985. Locomotor system. In Form and function in birds (eds King A. S., McLelland J.), pp. 57–147. London, UK: Academic Press. Search Google Scholar [38] Rayner J. V. M. 1988. Form and function in avian flight. In Current ornithology, vol. 5 (ed. Johnston R. F.), pp. 1–66. New York, NY: Plenum Press. Search Google Scholar [39] Reese, S., G. Dalamani, and B. Kaspers. 2006. The avian lungassociated immune system: a review. Vet. Res. 37: 311-324. [40] Ritchison, Gary. "Ornithology (Bio 554/754):Bird Respiratory System". Eastern Kentucky University. Retrieved 2007-06-27. [41] Roberts T. J., Marsh R. L., Weyand P. G., Taylor C. R. 1997. Muscular force in running turkeys: the economy of minimizing work. Science 275, 1113–1115. (doi:10.1126/science.275.5303.1113) [42] Rosser B. W. C., George J. C. 1986. The avian pectoralis: histochemical characterization and distribution of muscle fiber types. Can. J. Zool. 64, 1174–1185. (doi:10.1139/z86-176) [43] RSBP. 2003. Birds as biodiversity indicators for sustainability: a panEuropean strategy. [44] Spearman, R. I. C. 1966. The keratinization of epidermal scales, feathers, and hair. Biol. Rev. Cambridge Phil. Soc. 41: 59-96. [45] Stettenheim, P. 1972. The integument of birds. In: Avian biology, vol. II (D. S. Farner and J. R. King, eds.), pp. 1-63. Academic Press, New York, NLucas, A. M., and P. R. [46] Stettenheim, P. R. 2000. The integumentary morphology of modern birds – an overview. American Zoologist 40: 461-477. [47] Stettenheim. 1972. Avian anatomy. Integument. Agriculture Handbook 362, U.S. Department of Agriculture, Washington, D.C.Y. [48] Tobalske B. W., Hedrick T. L., Biewener A. A. 2003. Wing kinematics of avian flight across speeds. J. Avian Biol. 34, 177–184. (doi:10.1034/j.1600-048X.2003.03006.x [49] Vazquez R. J. 1995. Functional anatomy of the pigeon hand (Columba livia): a muscle stimulation study. J. Morphol. 226, 33–45. [50] Warrick D. R., Dial K. P. 1998. Kinematic, aerodynamic and anatomical mechanisms in the slow, maneuvering flight of pigeons. J. Exp. Biol. 201, 655–672 [51] Wing, Leonard W. (1956) Natural History of Birds. The Ronald Press Company.

[52] Williams, J. B. 1996. A phylogenetic perspective of evaporative water loss in birds. Auk 113: 457-472.

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