Leaf Mimicry in a Climbing Plant Protects Against Herbivory

Please cite this article in press as: Gianoli and Carrasco-Urra, Leaf Mimicry in a Climbing Plant Protects against Herbivory, Current Biology (2014), http://dx.doi.org/10.1016/j.cub.2014.03.010 Current Biology 24 Biology  24,, 1–4, May 5, 2014

ª2014

Elsevier Ltd All rights reserved

http://dx.doi.org/10.1016/j.cub.2014.03.010

Report Leaf Mimicry in a Climbing Plant Protects against Herbivory Ernesto Gianoli1,2,*  and Fernando Carrasco-Urra2 1 ´a,  Universidad de La Serena, Departamento de Biologı´a, Universidad Casilla 554, La Serena, Chile 2 ´ nica, Universidad de Concepcio ´ n, ´ n, Departamento de Bota´ nica, ´ n, Chile Casilla 160-C, Concepcio´ n,

Summary Mimicry Mimicry refers to adaptive adaptive similarity similarity between between a mimic mimic organism and a model model.. Mimicr Mimicry y in animal animals s is rather rather common, common, whereas documented cases in plants are rare, and the associated benefits are seldom elucidated [1, [1, 2]. We show the occurrence of leaf mimicry in a climbing plant endemic to a temperate temperate rainforest. rainforest. The woody vine   Boquila trifoliolata  mimics the leaves of its supporting trees in terms of size, shape, color, orientation, orientation, petiole petiole length, length, and/or and/or tip spininess. Moreover, sequential leaf mimicry occurs when a single individual vine is associated with different tree species. Leaves of unsupported vines differed from leaves of climbing plants closely associated with tree foliage but did not differ differ from from those those of vines vines climbi climbing ng onto onto leafles leafless s trunks trunks.. Consistent Consistent with an herbivoryherbivory-avoida avoidance nce hypothesis, hypothesis, leaf herbivory on unsupported vines was greater than that on vines climbing on trees but was greatest on vines climbing onto leafless trunks. Thus,   B. trifoliolata   gains protection against herbivory not merely by climbing and thus avoiding ground ground herbiv herbivore ores s [3] but but also also by clim climbi bing ng onto onto tree trees s whos whose e leaves are mimicked. Unlike earlier cases of plant mimicry or crypsis, in which the plant roughly resembles a background or color pattern [4–7 [4–7]] or mimics a single host [8, [8, 9],   is able to mimic several hosts. B. trifoliolata  is Results and Discussion Mimicry cases in plants are not common, and their adaptive value is rarely reported [1, [1, 2]. The most known example of  mimicry in plants occurs in Australian mistletoes, a group of  hemipa hemiparas rasitic itic plants plants whose whose leaves leaves mimic mimic those those of their  their  respective host tree species [8 [8]. The associated benefits or  ecological agents involved in this case of leaf mimicry are not clearly discerned [9 [9]. Floral mimicry in which pollinators are attracted and deceived [10, [10, 11] 11] has also been reported (mainly (mainly describing describing the resemblanc resemblance e between between two species). species). Other examples of mimicry or crypsis in plants include leaf  variegation variegation,, which is a whitish whitish mottling mottling that resembles resembles leaf  damage by mining larvae and may deter herbivores that avoid feedin feeding g or ovipos ovipositi iting ng on previo previousl usly y attack attacked ed leaves leaves [4], succulent Lithops succulent Lithops plants  plants that resemble stones in arid regions of Southern Africa [7 [7], and leaves [6 [6] or bracts [5 [5] that may make a plant cryptic against a leaf litter background. Even though though eviden evidence ce of mimicr mimicry y in plants plants has accum accumula ulated ted recently, it remains a rather contentious issue [1 [ 1]. The climbi climbing ng plant plant   Boquila trifoliolat trifoliolata a   (Lardizabalaceae) is endemi endemic c to the temper temperate ate rainfo rainfores restt of southe southern rn South South  America [12 12]. ]. Leaves of this twining vine are very variable in

*Correspondence: [email protected] *Correspondence:  [email protected]

size and shape and are composed of three leaflets that are pulvinated and therefore may change their orientation. Field observation observations s indicate indicate that  that   B. trifoliolat trifoliolata a   often often mimics mimics the leaves of its supporting trees in terms of size, shape, color, orientation, and vein conspicuousness, among other features ( Figure Figure 1 ). This phenomenon includes the display of a mucronate nate leaf leaf apex apex (a small small spine spine at the leaf tip) when twining twining around around a tree tree with with such such mucron mucronate ate leaves ( Figur F igure e 1 ); the botanical botanical description description of   of   B. trifoliolata   does not include this feature [14 [14]. ]. Unlike earlier mimicry reports, leaf mimicry mimicry by this this climbi climbing ng plant is confine confined d not to a single single species species but to several several host trees. Moreover, Moreover, when traversing traversing different different hosts, the same individual vine changes its leaf morphology accordingly ( Figure Figure S1 available S1  available online). To quantify this phenomenon, we compared 11 leaf traits from both B. both B. trifoliolata individuals and the tree species with which they were associated in a mature forest (45 vine individuals associated with 12 host tree species). We further evaluated whether leaf mimicry icry by this this vine vine was relate related d to herbiv herbivore ore avoida avoidance nce,, in analog analogy y to cryptic behavior against predators in animals. The statistical analysis (a mixed generalized linear model [GLM] with observations of tree leaf phenotype nested in species, which was a random factor) showed a significant association between the leaf phenotype of   B. trifoliolata and trifoliolata  and that of the supporting trees in 9 of the 11 leaf traits measured, including leaf and leaflet angle, leaf area and perimeter, leaflet petiole length, and leaf color ( Table T able 1 ). These patterns can hardly be explained by covariation of leaf phenotype with light availability because (1) the light environment of sampling sites wasrather wasrather homoge homogeneo neous us (4%–8%light (4%–8%light availa availabil bility ity), ), and(2) the host tree species, with contrasting leaf phenotypes, are not segregated across the light gradient [15 [15]. ]. Furthermore, leaves of prostr prostrate ate indivi individua duals ls of   B. trifoliolat trifoliolata a   (i.e., (i.e., those those vines vines growin growing g on the ground) ground) did not not differ differ from those those of vines vines that were climbing onto leafless stems or trunks (multivariate analysis of variance [MANOVA];   Table 2 ) but did differ from those climbing onto leafed individuals of the analyzed tree species (7 of 8 species, MANOVA; Table MANOVA; Table 2; 2;  Figure S2 ). Therefore, when there is no leaf to mimic, climbing plants are not different from plants growing unsupported, which show the ‘‘stand ‘‘standard’ ard’’’ leaf phenotype phenotype of the species. species. We also verified that individuals growing on bare tree trunks did differ from those growing on leafed tree hosts (6 of 8 species, MANOVA; data not shown; Figure shown;  Figure S2 ). S2 ). We found some field evidence supporting the hypothesis that leaf mimicry mimicry in climbing climbing individuals individuals of  B.   B. trifoliolata is related to herbivore avoidance. First, following the premise that indistinguishable phenotypes should lead to similar levels of leaf leaf dama damage ge [9], we found found in paired paired compar compariso isons ns that that herbivory did not differ between climbing vines and the supporting host trees (t138  = 21.712, p = 0.09; mean 6  SE of an herbivory herbivory index: vines 1.91 6   0.04 and trees 2.01 6   0.04). Second, leaf herbivory was significantly higher in creeping, unsupp unsupport orted ed indivi individua duals ls than than in those those climbi climbing ng on trees trees ( Figure Figure 2 ). Third, leaf herbivory on vine individuals climbing onto leafless supports—on which there is no leaf model to mimic— mimic—was was higher higher than than leaf leaf herbiv herbivory ory on unsup unsuppor ported ted individuals ( Figure Figure 2 ). Given that leafless stems conferred no protection protection,, these results suggest suggest that  that   B. trifoliolata trifoliolata   gains

Please cite this article in press as: Gianoli and Carrasco-Urra, Leaf Mimicry in a Climbing Plant Protects against Herbivory, Current Biology (2014), http://dx.doi.org/10.1016/j.cub.2014.03.010 Current Biology  Vol 24 No 9 2

Figure 1. Leaf Mimicry Mimicry in the Climbing Climbing Plant  Plant  Boquila trifoliolata Pictur Pictures es of the twiningvine twiningvine B. trifoliolata co-occurri co-occurring ng with woody species in the temperate temperate rainforest rainforest of southern southern Chile,where leaf mimicry mimicry in terms of size, color,and/orshap color,and/orshape e is evident evident.. White White arrowspoint arrowspoint to thevine (V)and to thehost tree tree (T). (T). Leaf Leaf lengthof lengthof thetree speciesis speciesis shown shown in parent parenthes heses es [13 13];thismay ];thismay help to estimate leaf size variation in the vine. (A) Myrceugenia (A)  Myrceugenia planipes (3.5–8 planipes  (3.5–8 cm). (B) Rhaphithamnus (B)  Rhaphithamnus spinosus (1–2 spinosus  (1–2 cm). (C) Eucryphia (C)  Eucryphia cordifolia (5–7 cordifolia  (5–7 cm). Notably smaller leaves of  B.   B. trifoliolata appear trifoliolata  appear to the left of the focus leaf. (D) Mitraria (D) Mitraria coccinea (a coccinea  (a woody vine; 1.5–3.5 cm). Both here and in (F), the serrated leaf margin of the model cannot be mimicked, but the vine shows one or  two indents. (E) Aextoxicon (E)  Aextoxicon punctatum (5–9 punctatum  (5–9 cm). (F)  (F)   Aristotelia chilensis (3–8 chilensis (3–8 cm). (G) Rhaphithamnus (G)  Rhaphithamnus spinosus (1–2 spinosus  (1–2 cm). (H) Luma apiculata apiculata (1–2.5cm).The (1–2.5cm).The inset inset shows shows more more clearl clearly y how B. trifoliolata trifoliolata hasa spiny spiny tip,like thesupportin thesupporting g treeletand treeletand unlike unlike allthe other other picture pictures s (and (and thebotanica thebotanicall descri descriptio ption) n) of this this vine. vine. SeealsoFigureS1 Seealso FigureS1 forpicturesshowi forpicturesshowing ng differe different nt leavesof leavesof thesameindividualof  thesameindividualof B. B. trifoliolata trifoliolata mimicking mimicking different different host trees.

protec protectio tion n agains againstt herbiv herbivore ores s not merely merely by climbi climbing ng and thus avoiding ground herbivores or by benefiting from associational resistance, as has been shown for other twining vines [3, 16, 17], 17], but also by climbing onto host trees whose leaves are mimicked. For crypsis to be a viable defensive strategy in plants, herbivores to be avoided should be visually orientated [2 [2]. The main main herbiv herbivore ores s in the study site are small small gastropods gastropods,, weevils, weevils, and leaf beetles beetles [18 18], ], whose whose foraging foraging behavior relies on both visual and olfactory cues [19–22 [19–22]. ].  A case of leaf mimicry in which its defensive role has been docum document ented ed is that that of leaf leaf varieg variegati ation.Thus,varieg on.Thus,variegate ated d leaves leaves were less attacked by herbivores than plain green leaves were in both a subcanopy liana [4 [4] and an understory herb [23 [ 23]] from

tropical tropical rainfores rainforests. ts. Likewise, Likewise, when vegetative vegetative bracts that resemb resemble le leaf leaf litter litter and cover cover reprod reproduct uctive ive stems stems in an  Appalachian herb were experimentally removed, herbivory increased and fruit set decreased [5 [5]. In the case of Australian mistletoes that mimic their hosts, protection against arboreal herbiv herbivore ores s (possu (possums) ms) had been been hypoth hypothesi esized zed [8], but no benefit benefit in terms terms of reduce reduced d herbiv herbivory ory has been been found found [9]. Nonetheless, mistletoe species mimicking host leaves have higher nitrogen levels (a proxy for palatability to herbivores) than than their their host host trees, trees, wherea whereas s nonmim nonmimick icking ing mistle mistletoe toes s show lower leaf nitrogen content than their hosts [24 [ 24]. ]. This sugges suggests ts that that mistle mistletoe toe mimicr mimicry y might might have have arisen arisen as an adaptive response against herbivory risk [9, [9, 24]. 24].

Please cite this article in press as: Gianoli and Carrasco-Urra, Leaf Mimicry in a Climbing Plant Protects against Herbivory, Current Biology (2014), http://dx.doi.org/10.1016/j.cub.2014.03.010 Leaf Mimicry in a Climbing Plant 3

Table 1. Relationships Relationships among Leaf Traits of the Climbing Plant Boquila Plant Boquila trifoliolata and trifoliolata  and Those of Its Supporting Trees Leaf Traits

Adjusted r2 

p

Maximum width Maximum length  Area Perimeter  Area:perimeter Thickness Leaf petiole length Leaflet petiole length Leaf angle Leaflet angle Color

0.49 0.54 0.63 0.60 0.07 0.15 0.58 0.25 0.23 0.62 0.32