Leaf Mimicry in the Climbing Plant Boquila trifoliolata Pictures of the twining vine B. trifoliolata co-occurring with woody species in the temperate rainforest of southern Chile, where leaf mimicry in terms of size, color, and/or shape is evident. White arrows point to the vine (V) and to the host tree (T). Leaf length of the tree species is shown in parentheses [13]; this may help to estimate leaf size variation in the vine. (A) Myrceugenia planipes (3.5–8 cm). (B) Rhaphithamnus spinosus (1–2 cm). (C) Eucryphia cordifolia (5–7 cm). Notably smaller leaves of B. trifoliolata appear to the left of the focus leaf. (D) Mitraria 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 punctatum (5–9 cm). (F) Aristotelia chilensis (3–8 cm). (G) Rhaphithamnus spinosus (1–2 cm). (H) Luma apiculata (1–2.5 cm). The inset shows more clearly how B. trifoliolata has a spiny tip, like the supporting treelet and unlike all the other pictures (and the botanical description) of this vine. See also Figure S1 for pictures showing different leaves of the same individual of B. trifoliolata mimicking different host trees. 

Leaf Mimicry in the Climbing Plant Boquila trifoliolata Pictures of the twining vine B. trifoliolata co-occurring with woody species in the temperate rainforest of southern Chile, where leaf mimicry in terms of size, color, and/or shape is evident. White arrows point to the vine (V) and to the host tree (T). Leaf length of the tree species is shown in parentheses [13]; this may help to estimate leaf size variation in the vine. (A) Myrceugenia planipes (3.5–8 cm). (B) Rhaphithamnus spinosus (1–2 cm). (C) Eucryphia cordifolia (5–7 cm). Notably smaller leaves of B. trifoliolata appear to the left of the focus leaf. (D) Mitraria 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 punctatum (5–9 cm). (F) Aristotelia chilensis (3–8 cm). (G) Rhaphithamnus spinosus (1–2 cm). (H) Luma apiculata (1–2.5 cm). The inset shows more clearly how B. trifoliolata has a spiny tip, like the supporting treelet and unlike all the other pictures (and the botanical description) of this vine. See also Figure S1 for pictures showing different leaves of the same individual of B. trifoliolata mimicking different host trees. 

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Mimicry refers to adaptive similarity between a mimic organism and a model. Mimicry in animals is rather common, whereas documented cases in plants are rare, and the associated benefits are seldom elucidated [1, 2]. We show the occurrence of leaf mimicry in a climbing plant endemic to a temperate rainforest. The woody vine Boquila trifoliolata mimi...

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... cases in plants are not common, and their adaptive value is rarely reported [1, 2]. The most known example of mimicry in plants occurs in Australian mistletoes, a group of hemiparasitic plants whose leaves mimic those of their respective host tree species [8]. The associated benefits or ecological agents involved in this case of leaf mimicry are not clearly discerned [9]. Floral mimicry in which pollinators are attracted and deceived [10, 11] has also been reported (mainly describing the resemblance between two species). Other examples of mimicry or crypsis in plants include leaf variegation, which is a whitish mottling that resembles leaf damage by mining larvae and may deter herbivores that avoid feeding or ovipositing on previously attacked leaves [4], succulent Lithops plants that resemble stones in arid regions of Southern Africa [7], and leaves [6] or bracts [5] that may make a plant cryptic against a leaf litter background. Even though evidence of mimicry in plants has accumulated recently, it remains a rather contentious issue [1]. The climbing plant Boquila trifoliolata (Lardizabalaceae) is endemic to the temperate rainforest of southern South America [12]. Leaves of this twining vine are very variable in size and shape and are composed of three leaflets that are pulvinated and therefore may change their orientation. Field observations indicate that B. trifoliolata often mimics the leaves of its supporting trees in terms of size, shape, color, orientation, and vein conspicuousness, among other features (Figure 1). This phenomenon includes the display of a mucronate leaf apex (a small spine at the leaf tip) when twining around a tree with such mucronate leaves (Figure 1); the botanical description of B. trifoliolata does not include this feature [14]. Unlike earlier mimicry reports, leaf mimicry by this climbing plant is confined not to a single species but to several host trees. Moreover, when traversing different hosts, the same individual vine changes its leaf morphology accordingly (Figure S1 available online). To quantify this phenomenon, we compared 11 leaf traits from 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 by this vine was related to herbivore avoidance, in analogy 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 asso- ciation between the leaf phenotype of B. 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 1). These patterns can hardly be explained by covariation of leaf phenotype with light availability because (1) the light environment of sampling sites was rather homogeneous (4%–8% light availability), and (2) the host tree species, with contrasting leaf phenotypes, are not segregated across the light gradient [15]. Furthermore, leaves of prostrate individuals of B. trifoliolata (i.e., those vines growing on the ground) did not differ from those of 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 2; Figure S2). There- fore, when there is no leaf to mimic, climbing plants are not different from plants growing unsupported, which show the ‘‘standard’’ leaf phenotype of the 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 S2). We found some field evidence supporting the hypothesis that leaf mimicry in climbing individuals of B. trifoliolata is related to herbivore avoidance. First, following the premise that indistinguishable phenotypes should lead to similar levels of leaf damage [9], we found in paired comparisons that herbivory did not differ between climbing vines and the supporting host trees (t 138 = 2 1.712, p = 0.09; mean 6 SE of an herbivory index: vines 1.91 6 0.04 and trees 2.01 6 0.04). Second, leaf herbivory was significantly higher in creeping, unsupported individuals than in those climbing on trees (Figure 2). Third, leaf herbivory on vine individuals climbing onto leafless supports—on which there is no leaf model to mimic—was higher than leaf herbivory on unsupported individuals (Figure 2). Given that leafless stems conferred no protection, these results suggest that B. trifoliolata ...
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... cases in plants are not common, and their adaptive value is rarely reported [1, 2]. The most known example of mimicry in plants occurs in Australian mistletoes, a group of hemiparasitic plants whose leaves mimic those of their respective host tree species [8]. The associated benefits or ecological agents involved in this case of leaf mimicry are not clearly discerned [9]. Floral mimicry in which pollinators are attracted and deceived [10, 11] has also been reported (mainly describing the resemblance between two species). Other examples of mimicry or crypsis in plants include leaf variegation, which is a whitish mottling that resembles leaf damage by mining larvae and may deter herbivores that avoid feeding or ovipositing on previously attacked leaves [4], succulent Lithops plants that resemble stones in arid regions of Southern Africa [7], and leaves [6] or bracts [5] that may make a plant cryptic against a leaf litter background. Even though evidence of mimicry in plants has accumulated recently, it remains a rather contentious issue [1]. The climbing plant Boquila trifoliolata (Lardizabalaceae) is endemic to the temperate rainforest of southern South America [12]. Leaves of this twining vine are very variable in size and shape and are composed of three leaflets that are pulvinated and therefore may change their orientation. Field observations indicate that B. trifoliolata often mimics the leaves of its supporting trees in terms of size, shape, color, orientation, and vein conspicuousness, among other features (Figure 1). This phenomenon includes the display of a mucronate leaf apex (a small spine at the leaf tip) when twining around a tree with such mucronate leaves (Figure 1); the botanical description of B. trifoliolata does not include this feature [14]. Unlike earlier mimicry reports, leaf mimicry by this climbing plant is confined not to a single species but to several host trees. Moreover, when traversing different hosts, the same individual vine changes its leaf morphology accordingly (Figure S1 available online). To quantify this phenomenon, we compared 11 leaf traits from 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 by this vine was related to herbivore avoidance, in analogy 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 asso- ciation between the leaf phenotype of B. 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 1). These patterns can hardly be explained by covariation of leaf phenotype with light availability because (1) the light environment of sampling sites was rather homogeneous (4%–8% light availability), and (2) the host tree species, with contrasting leaf phenotypes, are not segregated across the light gradient [15]. Furthermore, leaves of prostrate individuals of B. trifoliolata (i.e., those vines growing on the ground) did not differ from those of 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 2; Figure S2). There- fore, when there is no leaf to mimic, climbing plants are not different from plants growing unsupported, which show the ‘‘standard’’ leaf phenotype of the 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 S2). We found some field evidence supporting the hypothesis that leaf mimicry in climbing individuals of B. trifoliolata is related to herbivore avoidance. First, following the premise that indistinguishable phenotypes should lead to similar levels of leaf damage [9], we found in paired comparisons that herbivory did not differ between climbing vines and the supporting host trees (t 138 = 2 1.712, p = 0.09; mean 6 SE of an herbivory index: vines 1.91 6 0.04 and trees 2.01 6 0.04). Second, leaf herbivory was significantly higher in creeping, unsupported individuals than in those climbing on trees (Figure 2). Third, leaf herbivory on vine individuals climbing onto leafless supports—on which there is no leaf model to mimic—was higher than leaf herbivory on unsupported individuals (Figure 2). Given that leafless stems conferred no protection, these results suggest that B. trifoliolata ...

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... An individual Boquila vine that over the course of its rambling growth traversed the canopies of three hosts, mimicked each of them in their respective areas of proximity. 242 This finding led the original discoverers to speculate that volatile signals or horizontal gene transfer may underlie the mechanism by which the mimicry is achieved. These two hypotheses, however, were dashed by the discovery that B. trifoliolata leaves also mimic the "leaves" of artificial plastic plants, albeit not as well as they do the living forms of plants. ...
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... 22 Haberlandt's theory was tested experimentally 42 as well as supported by studies of a mimicking plant Boquila trifoliolata. 23,43,44 This plant has the intriguing ability to change the shape of its leaves according to the host plant. When plastic leaves were presented to Boquila trifoliolata, it changed the shapes of leaves from three-lobed leaves to longitudinal leaves, mimicking the plastic leaves too. ...
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... deem as cognitive abilities that undergird the potential for sui generis sentience, further research is necessary. 8 Still, some specific interesting behavioral examples include the demonstration of an advantage in foraging due to epigenetic memory of previous interactions in the case of clonal plants and the ability of the Boquila trifoliolata to mimic the leaves of its supporting host as a predation avoidance strategy (Gianoli & Carrasco-Urra, 2014). Moreover, the Venus flytrap's stimuli from its trigger hairs before closing possibly demonstrates numerical counting abilities (Böhm et al., 2016;. ...
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... Decne. (Lardizabalaceae) (Gianoli and Carrasco-Urra 2014). ...
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... Whereas mimicry is a well-known phenomenon in the animal kingdom, examples of true plant mimicry are less frequent, with documented cases in the plant literature being scarce (Niu et al., 2018;Lev-Yadun, 2016). An illustration nonetheless is provided by Gianoli and Carrasco-Urra (2014), who report that the leaves of Boquila trifoliolata can mimic the leaves of its supporting host, including size, shape, orientation, color, and petiole length, among other features. Moreover, the same individual can mimic two different hosts in a series. ...
... Two rival hypotheses are airborne VOC communication and horizontal gene transfer (Gianoli & Carrasco-Urra, 2014). However, taking into account that physical contact is not needed for mimicry to take place, a more radical hypothesis has recently been advanced: a plant-specific form of proto-vision akin to the ocelloid-based vision found in cyanobacteria and some dinoflagellates (cf. ...
... As we see it, what makes these instances of mimicry cognitively interesting is that they involve adaptations to the current contingencies of the environment. That the same exemplar of Boquila can tailor its phenotype to mimic different hosts (from different taxa) consecutively (Gianoli & Carrasco-Urra, 2014) invites explanations that prima facie resemble those invoked to account for the behaviors of some animal species (Lev-Yadun, 2016). ...
... 13 Individuals successfully attached to a support-tree improve their light intake, are more abundant and present higher biomass, physiological yield, reproductive output, and lower herbivory than those unattached. 12,47,[56][57][58][59][60][61] In woody climbers with adventitious roots, the plagiotropic (creeping) shoots and seedlings exposed to bright light, or even to low-light intensity, grew toward dark sites and moved away from light, exhibiting negative phototropism. 33,35,[38][39][40]42 In the chiaroscuro of the forest floor, potential support-trees have been found in the darkest sectors, 33 and under shady conditions, the climbing habit has also been found to be enhanced. ...
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... A further restriction on precise size estimation is imposed by the confounding effect of distance. Size comparisons are simple if the model and mimic are visible adjacent to each other, for example in the vine Boquila trifoliolata which mimics the leaves of the various tree species on which it grows (Gianoli and Carrasco-Urra 2014). If prey is seen in isolation, an assessment of size relies on being able estimate its distance from the observer. ...
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... The authors report that "Arabidopsis thaliana plants exposed to chewing vibrations produced greater amounts of chemical defenses in response to subsequent herbivory, and that the plants distinguished chewing vibrations from other environmental vibrations" (2014: 1258). 3. A study of the Boquilla trifoliolata, the climbing wood vine, demonstrates its ability to modify the appearance of its leaves to mimic the color, size, shape, and orientation of the host plant (Gianoli and Carrasco-Urra, 2014). Another study demonstrated that Arabidopsis thaliana seedlings are able to distinguish their neighbors by recognizing their body shapes (Crepy and Casal, 2015). ...
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... 94 The plant Boquila trifoliolata is able to mimic the neighboring plant leaves. 95 The capabilities of adaptation to their environment, communication, imitation or cooperation are used, among others, by ethologists to define animal intelligence. 96 In more general terms, the key issues underlying these capacities for perceiving information are: (i) the integration over time and space of these complex signals, their prioritization and the adoption of elaborate behaviors, 97 which should be addressed by a "phytoneurological" system according to 98, and (ii) the emergence of intentionality 75 or the ability to make choices involving consciousness. ...
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... www.nature.com/scientificreports/ and leaf mimicry has been established 8 . However, deciphering the mechanism behind the exceptional capacity of leaf mimicry in Boquila is indeed a challenging, complex task. ...
... Note that leaf mimicry is accomplished for both ovate leaves (study samples) and cordate-lobed leaves (inset) of the tree. For other cases of Boquila mimicking R. spinosus see 8,10 . ...
... We need to explain not only how Boquila is able to mimic over a dozen species in terms of leaf shape and size, even without direct contact, or how a single individual vine can mimic two different tree species 8 . We also need to elucidate how this vine can develop a small spine at the leaf tip when twining around-or being close to-species with such mucronate leaves, which include Luma apiculata 8 , Cissus striata 10 , and Rhaphithamnus spinosus (Gianoli, personal observations: a video footage showing this feature is included in the Supplementary Video S2); importantly, the botanical description of Boquila does not include spiny leaf tips 41 . ...
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The mechanisms behind the unique capacity of the vine Boquila trifoliolata to mimic the leaves of several tree species remain unknown. A hypothesis in the original leaf mimicry report considered that microbial vectors from trees could carry genes or epigenetic factors that would alter the expression of leaf traits in Boquila. Here we evaluated whether leaf endophytic bacterial communities are associated with the mimicry pattern. Using 16S rRNA gene sequencing, we compared the endophytic bacterial communities in three groups of leaves collected in a temperate rainforest: (1) leaves from the model tree Rhaphithamnus spinosus (RS), (2) Boquila leaves mimicking the tree leaves (BR), and (3) Boquila leaves from the same individual vine but not mimicking the tree leaves (BT). We hypothesized that bacterial communities would be more similar in the BR–RS comparison than in the BT–RS comparison. We found significant differences in the endophytic bacterial communities among the three groups, verifying the hypothesis. Whereas non-mimetic Boquila leaves and tree leaves (BT–RS) showed clearly different bacterial communities, mimetic Boquila leaves and tree leaves (BR–RS) showed an overlap concerning their bacterial communities. The role of bacteria in this unique case of leaf mimicry should be studied further.