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 ...
Context 2
... 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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... Decne. (Lardizabalaceae) (Gianoli and Carrasco-Urra 2014). ...
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Alseuosmia (Alseuosmiaceae) is an endemic New Zealand genus of small trees and shrubs, which is unusual in that some taxa appear to morphologically mimic unrelated species. The taxonomy of the group has long been debated with the extreme morphological diversity in A. banksii causing much of the confusion. Here we use ddRADseq to examine the genetic relationships between the species, with a particular focus on the morphological forms of A. banksii. Our analyses revealed that for species in the northern part of the distribution, genetic relationships largely matched geography rather than species’ boundaries based on morphology, and that hybridisation between morphs appears to be common. A diversity of morphologies is present within these northern Alseuosmia, including multiple forms that appear to mimic unrelated genera, and these may constitute a single gene pool. Further south, two species (A. turneri and A. pusilla) were genetically distinct in sympatry. We suggest maintaining the current taxonomy until further research can be undertaken.
... 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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A variety of traits is available for predators to distinguish unpalatable prey from palatable Batesian mimics. Among them, body size has received little attention as a possible mimetic trait. Size should influence predator behaviour if it shows variation between models and mimics, is detectable by the predator in question, and is not overshadowed by other traits more salient to the predator. Simple predictions within mimetic populations are that perfect mimics receive the lowest predation rate. However, prey body size is typically tightly linked to the nutritional yield and handling time for a successful predator, as well as likely being correlated with a model’s levels of defence. In certain circumstances, these confounding factors might mean that (a) selection pressures on a mimic’s size either side of the model’s phenotype are not symmetrical, (b) the optimal body size for a mimic is not necessarily equal to that of the model, and/or (c) for predators, attacking better mimics of a model’s body size more readily is adaptive. I discuss promising avenues for improving our understanding of body size as a mimetic trait, including the importance of treatments that range in both directions from the model’s size. Further work is required to understand how body size ranks in saliency against other mimetic traits such as pattern. Comparative studies could investigate whether mimics are limited to resembling only models that are already similar in size.
... 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.
... For instance, the two monophagous butterfly species Eurema brigitta and E. herla usually land on nonhost species with similar leaf shapes (Mackay & Jones, 1989). In a stimulating paper, Gianoli & Carrasco-Urra (2014) showed that by expressing leaf polymorphism, the woody vine Boquila trifoliolata mimics the leaves of its supporting trees that belong to different taxa. When a single individual vine climbs on different tree species, it mimics the leaf shape of each different supporting tree, thus having a sequence of location-and context-related leaf shapes. ...
... When a single individual vine climbs on different tree species, it mimics the leaf shape of each different supporting tree, thus having a sequence of location-and context-related leaf shapes. The unsupported vine parts and the parts that climb on leafless trunks have a different leaf shape from the shapes within canopies and suffer more damage from herbivory (Gianoli & Carrasco-Urra, 2014). The mechanism regulating this striking phenomenon is not only unknown but, if true, requires a very complicated visual or chemical sensing. ...
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... Seven years ago, Gianoli and Carrasco-Urra reported on their discovery of Boquila trifoliolata (Lardizabalaceae), a woody vine from temperate rainforests of southern Chile, capable of complex leaf mimicry, when leaves of up to three different host plants were mimicked by leaves of one B. trifoliolata plant. 1 However, according to a side-by-side published commentary, the absence of any plausible hypothesis for such a phenomenon makes this report unexplainable and mysterious. 2 Gianoli and Carrasco-Urra preferred some chemical volatile signals released from the host plants, which would allow the B. trifoliolata to mimic leaves of host plants. 1,3 As an alternative proposal, they also speculated that horizontal gene transfer between host plant and Boquila vine, mediated perhaps via airborne microbes, might allow this leaf mimicry. ...
... Seven years ago, Gianoli and Carrasco-Urra reported on their discovery of Boquila trifoliolata (Lardizabalaceae), a woody vine from temperate rainforests of southern Chile, capable of complex leaf mimicry, when leaves of up to three different host plants were mimicked by leaves of one B. trifoliolata plant. 1 However, according to a side-by-side published commentary, the absence of any plausible hypothesis for such a phenomenon makes this report unexplainable and mysterious. 2 Gianoli and Carrasco-Urra preferred some chemical volatile signals released from the host plants, which would allow the B. trifoliolata to mimic leaves of host plants. 1,3 As an alternative proposal, they also speculated that horizontal gene transfer between host plant and Boquila vine, mediated perhaps via airborne microbes, might allow this leaf mimicry. They proposed this scenario because B. trifoliolata leaves mimic the nearest foliage, irrespective if these leaves are from the host plants or some other neighboring plants. ...
... They proposed this scenario because B. trifoliolata leaves mimic the nearest foliage, irrespective if these leaves are from the host plants or some other neighboring plants. 1,3 The complexity of this mimicry, when B. trifoliolata leaves were shown to mimic shapes, colors, leaf orientations, petiole lengths, and vein conspicuousness and patterns may have a third hypothesis, totally different from the volatile signals from host plants or gene transfer via airborne microbes. This third hypothesis would support the possibility that plant vision based on plant ocelli 4,5 is behind this unique form of plant behavior. ...
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Upon discovery that the Boquila trifoliolata is capable of flexible leaf mimicry, the question of the mechanism behind this ability has been unanswered. Here, we demonstrate that plant vision possibly via plant-specific ocelli is a plausible hypothesis. A simple experiment by placing an artificial vine model above the living plants has shown that these will attempt to mimic the artificial leaves. The experiment has been carried out with multiple plants, and each plant has shown attempts at mimicry. It was observed that mimic leaves showed altered leaf areas, perimeters, lengths, and widths compared to non-mimic leaves. We have calculated four morphometrical features and observed that mimic leaves showed higher aspect ratio and lower rectangularity and form factor compared to non-mimic leaves. In addition, we have observed differences in the leaf venation patterns, with the mimic leaves having less dense vascular networks, thinner vascular strands, and lower numbers of free-ending veinlets.
... Whereas mimicry is a well-known phenomenon in the animal kingdom, examples of true plant mimicry are less frequent (Niu et al., 2018;Williamson, 1982), with documented cases in the plant literature being scarce (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. ...
... Although this has been previously observed in other species such as Australian mistletoes, in the case of B. trifoliolata, the lack of (physiological) connections in between vine and support, together with the impressive serial mimicking, somewhat reduces the alternative hypotheses as to what the mechanism that underlies mimicry in this species is (although see Pannell, 2014). In line with previous research, two alternative hypotheses are VOCs airborne 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 been recently advanced: a plant-specific form of proto-vision akin to the ocelloidbased type of vision found in cyanobacteria and some dinoflagellates (Baluška & Mancuso, 2016. ...
... 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). ...
Article
Full-text available
Unlike animal behavior, behavior in plants is traditionally assumed to be completely determined either genetically or environmentally. Under this assumption, plants are usually considered to be noncognitive organisms. This view nonetheless clashes with a growing body of empirical research that shows that many sophisticated cognitive capabilities traditionally assumed to be exclusive to animals are exhibited by plants too. Yet, if plants can be considered cognitive, even in a minimal sense, can they also be considered conscious? Some authors defend that the quest for plant consciousness is worth pursuing, under the premise that sentience can play a role in facilitating plant's sophisticated behavior. The goal of this article is not to provide a positive argument for plant cognition and consciousness, but to invite a constructive, empirically informed debate about it. After reviewing the empirical literature concerning plant cognition, we introduce the reader to the emerging field of plant neurobiology. Research on plant electrical and chemical signaling can help shed light into the biological bases for plant sentience. To conclude, we shall present a series of approaches to scientifically investigate plant consciousness. In sum, we invite the reader to consider the idea that if consciousness boils down to some form of biological adaptation, we should not exclude a priori the possibility that plants have evolved their own phenomenal experience of the world. This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition Philosophy > Consciousness Neuroscience > Cognition