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Plant Camouflage: Ecology, Evolution, and Implications
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Opinion
Plant Camouflage: Ecology, Evolution, and Implications Yang Niu,1 Hang Sun,1,* and Martin Stevens2,* Camouflage is a key defensive strategy in animals, and it has been used to illustrate and study evolution for 150 years. It is now evident that many camouflage concepts likely also apply to plants, attracting greatly increased attention. Here, we review the hypotheses and evidence for different camouflage strategies used by plants and conceptualise the state of play in plant concealment under a general framework of camouflage theory. In addition, we compare the camouflage strategies used by plants and animals, outline key factors promoting and constraining the evolution of concealment, and highlight the evolutionary and ecological implications of plant camouflage. Ultimately, we show how plant camouflage exhibits many commonalities with animals and how this understudied parallel phenomenon can inform key questions in ecology and evolution.
Highlights There is clear evidence that plants use camouflage as a defensive strategy. Plants use many camouflage strategies, hindering predator detection and/or recognition. Plant camouflage exhibits many ecological and evolutionary commonalities with animals. Plant camouflage is a key factor in adaptation to different habitats and population divergence. Various factors constrain and facilitate the evolution of camouflage in plants.
The Natural History of Plant Camouflage Colour mediates numerous important interactions between organisms and their environments [1]. Possibly owing to our attraction to bright flowers and fruits, our understanding of plant coloration in the context of plant–animal interactions is mostly limited to their reproductive functions (e.g., attracting pollinators and seed dispersers [2,3]). However, plants also need to defend themselves against their enemies (herbivores and other antagonists), which often locate targets visually [4]. While it is well established that animals use colour in various defensive strategies [5,6], the potential defensive functions of plant coloration have often been neglected. In a paper on coloration, Wallace wrote that ‘plants rarely need to be concealed, and obtain protection either by their spines, their hardness, their hairy covering, or their poisonous secretions’ [7]. Such assumptions might be a major reason why plant camouflage received little attention. However, today there is a growing acknowledgement that many plants use camouflage to protect themselves from their enemies, and they use a striking range of strategies to do so, from resembling objects such as stones to matching the colour of the environment. This appreciation expands our understanding of plant defensive strategies and the evolution of plant coloration. More importantly, plant concealment provides a parallel system to animals, with the study of camouflage widely used to inform various key issues in ecology and evolution. It is likely that other colour-related defensive strategies, such as mimicry and aposematism, which have also received limited attention [8,9], are also found in plants. However, here we focus on camouflage. Camouflage is a concept traditionally used in zoology that refers to an assemblage of strategies that make detection or recognition more difficult [10]. Scattered anecdotes of camouflaged plants have been reported for almost 200 years. For example, Burchell documented how members of the genus Mesembryanthemum (Aizoaceae) in southern Africa ‘in colour and appearance bore the closet resemblance to the stones between which it was growing’ to ‘escape the notice of cattle and wild animals’ [11]. The resemblance of Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
Plant camouflage provides a novel testing ground for key questions in ecology and evolution.
1 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, 650201, Kunming, Yunnan, China 2 Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall, TR10 9FE, UK
*Correspondence: [email protected] (H. Sun) and [email protected] (M. Stevens).
https://doi.org/10.1016/j.tree.2018.05.010 © 2018 Elsevier Ltd. All rights reserved.
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mistletoes to their host plants has also long been regarded as an adaptation to avoid herbivores [12]. In 1978, Wiens collated many putative examples of resemblance to dead grass, sticks, or stones under the term mimicry [13], although many of these examples should now be regarded as masquerade [8] (see below). More potential cases have been added by Lev-Yadun, as well as other potential defensive functions of coloration [8]. However, work on plant camouflage has been almost entirely descriptive, until more rigorous studies in the past few years have combined techniques in colour measurement [14,15] and knowledge of animal colour vision [16,17] with experimental evidence (see below). It is now clear that several camouflage strategies used by animals apply to plants, with similar key ecological and evolutionary processes and their implications.
A Framework for Understanding Camouflage: Animal Concepts Applied to Plants Here, we outline the main strategies of camouflage that have been identified (for definitions and examples, see Box 1) and discuss comparable cases in both animals and plants (Figure 1; Table S1 in the supplemental information online). These include various types of crypsis to prevent detection and masquerade to hinder recognition and/or classification, plus strategies such as using materials from the environment in decoration [10]. Several strategies for crypsis exist, including matching the background, using disruptive coloration to destroy key body edges and features, and countershading to hide shadows,
Box 1. Key Camouflage Strategies and How They Work For examples of the use of these strategies in animals and putative cases in plants, see Table S1 in the supplemental information online. Background matching works when the bearer generally matches the colour, lightness, and pattern of one (specialist) or several (compromise) background types [10,71]. Disruptive coloration involves a set of markings that create the appearance of false edges and boundaries and hinder the detection or recognition of an object’s, or part of an object’s, true outline and shape [10,72]. Self-shadow concealment and obliterative shading are strategies where directional light, which would lead to the creation of shadows, is cancelled out by countershading [10,73,74] and where countershading leads to the obliteration of 3D form [10]. Distractive markings direct the ‘attention’ or gaze of the receiver from traits that would give away the animal (such as the outline), or interfere with visual mechanisms that an observer could use to detect or recognise an object by virtue of the distractive markings’ high-contrast or conspicuousness [75]. This strategy is controversial [75,76]. Masquerade is a strategy where recognition is prevented by resembling an uninteresting object, such as a leaf or a stick [10], and a masquerading species as one whose appearance causes its predators or prey to misclassify it as a specific object found in the environment, causing the observer to change its behaviour in a way that enhances the survival of the masquerader [77]. Therefore, it is different from forms of crypsis that prevent detection in the first instance. Note that masquerade shares similarities with some other defences, including Batesian mimicry, but they are generally treated as distinct strategies in mechanism and implications. Batesian mimicry involves a mimic resembling a potentially harmful model organism that a predator would normally avoid (such as a hoverfly resembling a wasp). Masquerade, however, involves matching a model that is not normally of interest to the predator, such as a non-living inanimate object such as a stone, or a background object such as a twig. As a consequence, Batesian mimicry might increase the attack rate of a predator on the model species, while masquerade does not. Decoration relates to an organism that (by means of specialist behaviour and/or morphology that has been favoured by selection for that purpose) accumulates and retains environmental material that becomes attached to the exterior of the decorator [30].
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Plant
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(E) No known analogue
(F) No known analogue
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Figure 1. Key Camouflage Strategies in Animals and Plants. (A, B) A juvenile horned ghost crab (Ocypode ceratophthalma, A) and an alpine Corydalis plant (Corydalis benecincta, B) use background matching to blend with the background. (C,D) Juvenile shore crab (Carcinus maenas, C) and seeds of cowpea (Vigna unguiculata, D) can use disruptive colours to hinder the detection of true outline. (E) Eyed hawk moth caterpillar (Smerinthus ocellata, E) has body colours that cancel out the shadows created by directional light (no analogous example has yet been proposed in plants). (F) The white comma mark on the hind wing of comma butterfly (Polygonia c-album, F) has been suggested to be a distractive mark that directs the attention of the receiver from the body outline (no analogue has been proposed in plants yet). (G,H) Young caterpillars of swallowtail butterfly (Papilio sp., G) resemble bird droppings as an example of masquerade, and the living stone plant (Lithops terricolor, H) is widely suggested as a masquerader. (I,J) The long-legged spider crab (Macropodia rostrata, I) decorates itself with seaweeds, and a potential analogue in plants are some coastal plants, passively decorated by sand (e.g., seedlings of Silene sp., J), decreasing their conspicuousness. Photo credits: (A, C, E, G, I) Martin Stevens, (B) Yang Niu, (D) Lian-Yi Li, (F) Jiong-Ao Yang, (H) Keith Green, (J) Simcha Lev-Yadun. See also Table S1 in the supplemental information online.
DecoraƟon
Masquerade
DistracƟve mark
Countershading
DisrupƟon
Background matching
Animal
plus other more debatable concepts (Box 1; Figure 1). Many of these strategies are likely used by plants, too (Table S1). Matching the colour of natural habitats (e.g., leaf litter, bare or rocky ground) is likely in various adult plants [18–20] (Figure 1B), juveniles [21–24], and seeds [25–27] (and even flowers and fruits [28,29]). For disruptive coloration, many seeds have high-contrast spots and stripes that subjectively destroy their outline [8] (Figure 1D). Furthermore, many animals decorate themselves for concealment with objects from their environment [30], and although plants cannot do this actively, some are suggested to obtain a cryptic appearance through passively acquiring decoration materials in certain environments. For example, some coastal and dune plants become covered by sand grains because of their sticky glandular trichomes, thereby making them less conspicuous [31].
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Masquerade acts to prevent recognition, rather than detection, by resembling unimportant objects in the environment that a predator would normally ignore [30]. Analogous to caterpillars matching dead twigs, living stones [32], cacti [13], passion vines [33], mistletoes [34], and certain other cases provide putative examples of masquerade in plants [35] (Table S1), although sometimes the distinction with mimicry and background matching can be complex. Otherwise, across animals there seems to be a greater range of camouflage types than likely occurs in plants, but it is unclear whether this is because they incur fewer constraints (see below), or because much diversity of camouflage in plants is still undiscovered (see [8]).
Current Evidence for Camouflage in Plants While subjective evidence for plant camouflage is often compelling, experimental testing and objective studies are required. A premise that plant camouflage occurs is that visual cues are an important sensory mechanism used by putative enemies (usually insects). Studies often take this as self-evident, but it is important to pay close attention to the natural history of the study system and consider alternative mechanisms, such as olfaction [36]. However, under this premise, first, plant targets should be hard to detect or recognise by antagonists, rather than by humans; and second, plants should obtain higher net fitness through camouflage. Otherwise, since plant coloration might have alternative functions (Box 2), experiments that dissect different (often nonexclusive) hypotheses are needed. Are Plants Camouflaged to Relevant Observers? Vision varies greatly among species, so assessing camouflage requires methods that account for receiver perception [15]. Using advances in measurement technology and knowledge of animal vision, recent studies have verified that plants can be concealed. Approaches have involved either simple comparison of reflectance spectra of plants and the background [18,23,24] or advanced colour vision discrimination models [19–22]. For example, the reflectance of cryptic-coloured bracts of Monotropis odorata is very similar to that of the surrounding leaf litter [18]. In addition, colour information from calibrated images has been used to test the similarity between leaves [24] and seeds [27] with soil substrates. While objective quantification is useful, where possible it is often preferable to consider the vision of the receiver. A specific animal colour vision model (of a herbivorous bird) was first used to verify the resemblance between juvenile leaves of two New Zealand plants (Pseudopanax carssifolius and Elaeocarpus hookerianus) and the leaf litter surroundings [21,22]. A butterfly vision model was also used to quantify colour similarity between two alpine Corydalis plants and their rock backgrounds [19,20]. However, the parameters for these models are often only available for a limited number of animal species, and some plants are consumed by several herbivore groups [24], making it difficult to always use a specific model. So far, most work on plant camouflage has clearly focussed on background matching, regarding colour similarity to substrates. Studies of other types of camouflage, most notably masquerade and disruptive coloration, are very rare. Beyond colour, the leaves of many plants also appear to resemble the size and shape of elements in the environment [37], affording potential masquerade, but quantitative examination is rare. Given that various methods have been developed in animals to quantify visual appearance (e.g., [14,38–40]), further studies on plant camouflage can utilise such approaches. Furthermore, manipulative experiments and tests of receiver detection rates are needed to demonstrate camouflage unequivocally (see below).
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Box 2. Anthocyanin and Camouflage Colour in Plants Anthocyanin is the most important pigment class that contributes to non-green plant colours, including not only bright flowers and fruits but also cryptic seeds and leaves [78]. Different content and types of anthocyanin, and their combination with other pigments (e.g., chlorophyll) and optical structures, can produce various camouflaged colours ([19,20]; Figure IA,B). The accumulation of anthocyanin can be induced by abiotic environment stress, such as strong light, drought, soil salinity, or phosphorus deficiency, and thus might have potential physiological functions in addition to the ecological functions [53]. The light-screening (photoprotection) hypothesis has received most attention recently, according to which anthocyanins can relieve photo-oxidative stress by protecting leaf tissues from harmful effects of light at low temperatures and under other conditions [9,53,79]. This hypothesis can be tested in camouflaged plants by comparing the physiological parameters between different pigment morphs in some polymorphic systems [19]. Nevertheless, such an explanation is not sufficient to explain why some non-photosynthetic organs, for example, seeds and flowers, are also apparently camouflaged due to anthocyanin accumulation. In addition, the accumulation of anthocyanin may accompany increasing chemical defence because they share some common metabolic pathways [80]. Therefore, it is possible that some apparent camouflage colours instead or additionally reflect anthocyanin accumulation accompanied by increasing chemical defence. This explanation is not difficult to test by analysing the actual relationship between these two aspects in camouflaged plants. However, we note that not all camouflage colours involve anthocyanin pigments (Figure IC, D).
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Figure I. Many Camouflaged Leaf Colours, Such as Those in Corydalis hemidicentra (A), Are Formed by Anthocyanins Combined with Other Pigments (e.g., Chlorophyll (B). Plant camouflage can also be achieved without anthocyanin, for example, the scarious bracts of Monotropsis odorata (C) and the silky-lanate hairs covering Saussurea medusa (D). Picture credits: (A, B, D) Yang Niu, (C) Jim Fowler.
Do Plants Obtain Higher Fitness through Camouflage? Higher fitness via concealment might arise from reduced damage rates and higher survivorship and reproductive success. However, it is challenging to examine these advantages in the field for at least two reasons. First, current phenotype may be a result of selection history, with the key enemies now absent [21,22]. Second, it can be difficult to set a proper control, as any artificial changes in colour might introduce unwanted confounds (e.g., changed growth or smell). Nevertheless, some studies have addressed this issue. Using various coloured pine (Pinus sylvestris) seeds combined with natural substrates of different colours, work has shown that seeds with colours that better matched the substrate had lower predation risk from birds [26]. In a more recent study, Strauss and Cacho [24] artificially changed the substrate of cryptic plants of Streptanthus breweri, making them more conspicuous to potential herbivores, which increased damage compared with control plants. This is a clever treatment that increased mismatching without changing the plant itself, but the authors acknowledged that this could change thermal conditions and influence herbivore behaviour [24]. Taking advantage of leaf colour dimorphism in Corydalis benecincta, Niu et al. [19] found that the more camouflaged morph had higher survivorship than a green
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morph in two of three populations studied. While natural dimorphism provides an ideal comparison in this system, more experiments are needed to exclude the potential effect of chemical differences that relate to leaf colour. Other Evidence: Divergence and Convergence In general, patterns of divergence and convergence can provide further evidence of the evolution of plant camouflage. First, because the efficacy of camouflage is environment specific, we expect divergence in camouflage between allopatric populations. Multiple mechanisms can be involved here, depending on the specific species, including genetic adaptation or colour change over various timescales, as well as ontogenetic changes in appearance linked with changes in life history. In animals, there are many examples of differences in camouflage appearance between populations driven by genetic adaptation, such as in mice [41] and lizards [42]. The degree of association can be mediated by levels of migration and gene flow [42]. In species capable of colour change, individuals from the same genetic population can adopt appearances linked to the environment where they settle or develop (e.g., sand fleas [43] and crabs [44]). Some animals also undergo ontogenetic changes linked to differences in habitat use and predator risk [45]. In plants, a significant divergence of seed camouflage colour was reported in a bean (Acmispon wrangelianus) in California between two soil types, namely, serpentine and nonserpentine, and even between sites within the same soil type but of different colour [27]. Given that gene flow is likely because of close distances between sites, this divergence implied strong natural selection on seed colour [27]. More recently, divergence in camouflage leaf colour was found between populations with different rock colours in Corydalis hemidicentra, matching their home background better than others [20] (Figure 2). In contrast to the seed example, this divergence could be consolidated by the isolated habitats produced by the mountainous landscape [20,46]. A similar pattern was also found in leaf colours of S. breweri, which are closer to their home substrates than to other substrates [24], although this was not highlighted by the authors as an adaptive divergence. We also note that there is great intraspecific colour variation between populations of the living stone (genus Lithops), which is thought to be associated with local matches between plants and substrates [47]. These specific local camouflage effects (through background matching) across populations are difficult to explain by alternative nonadaptive hypotheses. In contrast to divergence, unrelated species converge on similar form for camouflage when living in the same visual environment. Numerous animals show similarities in appearance associated with habitat, including, for example, rodents [48] and lizards [42]. Most studied
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Figure 2. Convergence and Divergence in Plant Camouflage. (A) Convergence in camouflage colour between Fritillaria delavayi (Liliaceae, top) and Saussurea quercifolia (Asteraceae, bottom) in alpine screes (with limestone substrate) from Southwest China. (B) Divergence in camouflage leaf colour among populations of Corydalis hemidicentra. Picture credits: (A) Hang Sun, (B) Yang Niu.
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cases are due to genetic mechanisms [48,49], but similarities could equally arise in different species of organism that are all capable of plasticity (e.g., crustaceans). In plants, a brief survey of the local flora of New Zealand and North America found descriptive evidence of convergent plant colours that match the substrates [50]. A similar convergence has also been found in the alpine plants of Southwest China (Figure 2; see [19]). Furthermore, many plants in sandy environments are suggested to have similar pale colours through different mechanisms [31]. However, no rigorous tests have yet been conducted to examine these phenomena.
What Factors Constrain or Promote the Evolution of Plant Camouflage? Costs and Constraints on Plant Camouflage Evolution Compared with animals, cases of camouflaged plants are seemingly less common, and the types of camouflage strategies are also apparently less diverse. This might be because until recently, plant camouflage had not been studied regularly, or it could be due to intrinsic differences between plants and animals. Camouflage incurs inevitable physiological and ecological costs in animals [5], but costs and constraints might be more considerable in plants (especially for their shoots). At least three general classes of limitation, that is, in physiology, camouflage efficacy, and selection strength, might hinder the evolution of plant camouflage (Table S1). Different from many animals, most plants are autotrophic and have to be green (the colour of chlorophyll) to live via photosynthesis. This is likely to be one reason why certain camouflage strategies used by animals, such as transparency, have not been found in land plants. Furthermore, any non-photosynthetic pigment might decrease photosynthetic performance [51,52] and thereby influence the fitness of the whole plant. For example, in a number of redleaved plants there seem to be costs of being non-green in photosynthesis [52–54]. In colourdimorphic C. benecincta, however, the rock-like morph and the green morph share similar photosynthetic performance [19]. Possibly due to restrictions on finding suitable study systems, work addressing potential costs and constraints is still rare and needs further attention. Plants cannot escape in most of their life stages and therefore can be located and attacked by enemies repeatedly. For the same reason, enemies can learn to detect or recognize them (as also suggested by Williamson [55]). In addition, plants cannot choose microhabitats that optimize their camouflage actively, as some animals do [56], which can improve camouflage. In turn, most flowering plants need to attract pollinators for reproduction, and their flowers may inevitably decrease camouflage efficacy. However, these arguments are not entirely convincing because many animals also use conspicuous sexual signals, and one can argue that because plants cannot escape, their need for camouflage should be greater, not lower. A majority of plants are modular organisms composed of numerous similar structures (e.g., leaves and flowers), which is not the case for many animals. Given this, many mature plant individuals can be more robust (to tolerate and survive attack and regrow), such that selection might be not as strong as it is in animals to induce any fitness advantage conferred by camouflage. Differences in structure between plants and animals might also influence their general appearance, potentially another reason why some camouflage strategies, such as countershading, have not been found in plants. Factors That May Facilitate Plant Camouflage Evolution Camouflage will have higher opportunity to evolve when the above-mentioned constraints are weak or broken, such as in plants that do not rely on photosynthesis. Monotropis odorata [18] (see Figure IC in Box 2) and other heterotrophic plants [57] are potential examples. The specific Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
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life stage of a plant, such as its seeds (when photosynthesis is not necessary), might also provide better candidates to expect camouflage. To break the latter two constraints (low camouflage efficacy and low selection strength), specific habitats and sizes (or ages) of plants might be favoured. An open habitat not only increases the pressure of visual selection [20,50,58] but also facilitates better camouflage by providing no landmarks for enemies to locate targets. Each individual can also incur a higher risk of damage (stronger selection strength) in such habitat due to low plant density. In addition, small plants could obtain better camouflage for two reasons. First, they are inconspicuous per se compared with larger plants. Second, backgrounds are often more diversified at smaller size scales, providing complex visual environments that are known to facilitate camouflage [59]. Meanwhile, selection on small plants should be stronger because they are more fragile. Consistent with this idea, camouflage has often been found in either small herbs [18–20,24] or the fragile stages of plant life history, such as juveniles [21–23] and seeds [25–27]. This again parallels many animal systems, where juveniles are often apparently more concealed than adults. Overall, stronger selection has been shown to facilitate the evolution of camouflage in plants. For example, cryptic-coloured plant species were found to suffer seven times more damage than the normal green species in some flora [50]. Improved camouflage efficacy was found to associate with higher damage risk among populations of C. hemidicentra [20]. Furthermore, specialized enemies might impose stronger selection compared with generalists, since they can overcome or even utilise the plant’s chemical defences [60], forcing hosts to evolve alternative defensive strategies. For example, butterfly specialists are suggested to be the main selective agent in several camouflaged plant genera, including Corydalis (Apollo butterflies [19,20]), Streptanthus (pierid butterflies [24,26]), and Passiflora (Heliconius butterflies [33]). It is interesting to note that mistletoes, a resemblance system that still attracts debate [61,62], are also important host plants of some butterflies [34], which have been neglected as a potential selection pressure for a long time [63]. Collectively, current evidence suggests that heterotrophism, open habitats, small individual size, fragile structure, and specialized enemies might facilitate the evolution of plant camouflage.
Other Key Ecological and Evolutionary Issues Regarding Plant Camouflage Evolutionary Consequences of Camouflage Camouflage can place considerable selection pressure on enemies, which can often manifest as changes in enemy search behaviour or perceptual mechanisms. In animals, predators are thought to adopt search images for camouflaged prey [64], involving heightened attention toward recently encountered or common prey. A key outcome can be negative frequencydependent (apostatic) selection [65], whereby common morphs are found disproportionately often compared to rarer morphs, leading to a selective advantage of rare forms. This can favour prey polymorphism and fluctuations in morph frequency over time. Overall, many animals are polymorphic, and this has been studied in snails [66], moths [67], and other organisms both in the context of matching different backgrounds and apostatic selection. Other work has demonstrated how search images occur in predators and link to diversity in prey appearance in computer experiments [65]. Studying search images and the reasons for polymorphism in the wild is notoriously difficult, however. In plants, it is entirely possible that these processes occur and lead to polymorphism in camouflage appearance (see the dimorphic leaf colour in C. benecincta [19]). The work of Nystrand and Granstrom [26] found 8
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that bird predation can drive or maintain colour dimorphism in seed camouflage, possibly through search image mechanisms. In contrast to search images and apostatic selection, intraspecific diversity may arise if selection favours individuals that match different patches in the same location. Across populations, specific local matching can hinder migration between populations because of potentially higher mortality induced by mismatching intermediate forms. This process can decrease gene flow between populations and thus consolidate divergence in colour and other characters. It could even promote speciation, as indicated in some animals, for example, stick insects [68]. Alternatively, a compromise or generalist camouflage can arise and allow migration between habitats with different colours. When individuals are potentially seen in multiple visual environments or patches of different appearance, individuals may utilise an intermediate or generalist appearance between multiple background types while matching none perfectly. Some experiments in artificial systems show that compromise camouflage could work (e.g., [69]), but this has not yet been demonstrated in real animals. In plants, this strategy has been implied in C. hemidicentra, where camouflage is not so specialist but apparently resembles several backgrounds [20]. Compromise camouflage could also occur in the dispersal stages (e.g., seeds), when they might face different habitats or backgrounds. In general, much theory has been developed regarding the evolution of specialist versus generalist camouflage strategies in mobile animals, and it will be important explore these ideas in plants. Potential Influence of Human Activity on the Evolution of Plant Camouflage Humans have a major influence on the natural world, and this includes several examples of camouflage (e.g., industrial melanism and the peppered moth [67] and climate change and snowshoe hares [70]). In plants, commercial harvesting could be a major selection pressure. For instance, commercial harvests in the Himalayas are suggested to explain the dwarfing process of Saussurea laniceps in the past 100 years. We have recently noticed that the putative camouflage of the traditional medicinal plant Fritillaria delavayi may correlate with the strength of selection by commercial harvests in Southwest China and neighbouring regions. A similar process might also be happening in South Africa on living stones, which have suffered heavily from commercial collection [32]. Given rapid human-induced changes, it is valuable to test whether and how human activities influence the evolution of camouflage in these plants, and their consequences.
Concluding Remarks It has long been known that colour is important in the communication between flowers and pollinators, and now it is apparent that plants use colour to hide from enemies, too. Camouflage has been documented in a number of plants from different continents, the efficacy and fitness of which have been verified in some cases, with the evolutionary process either illustrated or implied. Although studies are still limited, there are noticeable factors that facilitate the evolution of plant camouflage. However, we are at the beginning of this field, and more experimental studies are needed to uncover generalities and to answer many unsolved questions (see Outstanding Questions). Nevertheless, there is a wealth of theory and concepts from animal camouflage to utilise, where the evolution, mechanisms, and efficacy of camouflage are attracting the attention of evolutionary biologists, behavioural biologists, psychologists, vision scientists, and others. The emerging picture of plant appearance is that plants do far more than entice pollinators and photosynthesise with their colours, but we now need to discover just how important a role camouflage has in their ecology and evolution, and to their enemies.
Outstanding Questions What mechanisms enable plant camouflage? Camouflage form can stem from genetic mechanisms or from phenotypic plasticity. The specific mechanism, and its flexibility, can have a major influence on the nature of camouflage and its implications, and how organisms respond to spatial and temporal uncertainty [81]. Reciprocal transplantation and common garden experiments will be valuable to test the relative importance of these two mechanisms in plants. Is there a conflict between strategies toward friends versus enemies and how can it be solved? The trade-off in animals between camouflage and sexual signals has been a subject of long-standing study (e.g., [82,83]). This trade-off might also exist in plants that need to attract pollinators as well as avoid enemies. Using different sensory modalities [18] and phenological mismatches [19] between them can be possible solutions. How common is camouflage in plants? Although many putative camouflage cases have been suggested [8,13,37,84], more studies are needed to examine them, especially for strategies other than background matching. Based on these studies, we can estimate the geographic and phylogenetic distribution of plant camouflage and the factors driving plant evolution using comparative studies. How important is camouflage for plants? Plants adopt various defensive strategies. It will be valuable to investigate the relationship between camouflage, other defensive coloration strategies (e.g., aposematism), other non-colour defences (e.g., physical and chemical defences), and when and why different defences evolve. What are the evolutionary consequences of plant camouflage? There is much to learn regarding how phenotypic polymorphism, genetic isolation, and even speciation can be influenced by the evolutionary process of plant camouflage. Could the evolution of plant camouflage be influenced by human selection? Direct commercial harvesting can be a strong selective pressure on the evolution of wild animals [85], which might also influence the visual characters of
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Acknowledgements We thank Keith Green, Jim Fowler, Simcha Lev-Yadun, Lian-Yi Li, and Jiong-Ao Yang for generously providing images. We thank Tim Caro and Simcha Lev-Yadun for helpful comments on the manuscript. This work was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (XDA 20050203 to H.S.)，Major Program of the NSFC (31590823 to H.S.), the National Key R & D Program of China (2017YF0505200 to H.S.), NSFC (31670214 to Y.N.), Yunnan Applied Basic Research Projects (2016FB035 to Y.N.), and Youth Innovation Promotion Association, CAS (2018427 to Y.N.).
Supplemental Information Supplemental information associated with this article can be found online at https://doi.org/10.1016/j.tree.2018.05.010.
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Opinion
Plant Camouflage: Ecology, Evolution, and Implications Yang Niu,1 Hang Sun,1,* and Martin Stevens2,* Camouflage is a key defensive strategy in animals, and it has been used to illustrate and study evolution for 150 years. It is now evident that many camouflage concepts likely also apply to plants, attracting greatly increased attention. Here, we review the hypotheses and evidence for different camouflage strategies used by plants and conceptualise the state of play in plant concealment under a general framework of camouflage theory. In addition, we compare the camouflage strategies used by plants and animals, outline key factors promoting and constraining the evolution of concealment, and highlight the evolutionary and ecological implications of plant camouflage. Ultimately, we show how plant camouflage exhibits many commonalities with animals and how this understudied parallel phenomenon can inform key questions in ecology and evolution.
Highlights There is clear evidence that plants use camouflage as a defensive strategy. Plants use many camouflage strategies, hindering predator detection and/or recognition. Plant camouflage exhibits many ecological and evolutionary commonalities with animals. Plant camouflage is a key factor in adaptation to different habitats and population divergence. Various factors constrain and facilitate the evolution of camouflage in plants.
The Natural History of Plant Camouflage Colour mediates numerous important interactions between organisms and their environments [1]. Possibly owing to our attraction to bright flowers and fruits, our understanding of plant coloration in the context of plant–animal interactions is mostly limited to their reproductive functions (e.g., attracting pollinators and seed dispersers [2,3]). However, plants also need to defend themselves against their enemies (herbivores and other antagonists), which often locate targets visually [4]. While it is well established that animals use colour in various defensive strategies [5,6], the potential defensive functions of plant coloration have often been neglected. In a paper on coloration, Wallace wrote that ‘plants rarely need to be concealed, and obtain protection either by their spines, their hardness, their hairy covering, or their poisonous secretions’ [7]. Such assumptions might be a major reason why plant camouflage received little attention. However, today there is a growing acknowledgement that many plants use camouflage to protect themselves from their enemies, and they use a striking range of strategies to do so, from resembling objects such as stones to matching the colour of the environment. This appreciation expands our understanding of plant defensive strategies and the evolution of plant coloration. More importantly, plant concealment provides a parallel system to animals, with the study of camouflage widely used to inform various key issues in ecology and evolution. It is likely that other colour-related defensive strategies, such as mimicry and aposematism, which have also received limited attention [8,9], are also found in plants. However, here we focus on camouflage. Camouflage is a concept traditionally used in zoology that refers to an assemblage of strategies that make detection or recognition more difficult [10]. Scattered anecdotes of camouflaged plants have been reported for almost 200 years. For example, Burchell documented how members of the genus Mesembryanthemum (Aizoaceae) in southern Africa ‘in colour and appearance bore the closet resemblance to the stones between which it was growing’ to ‘escape the notice of cattle and wild animals’ [11]. The resemblance of Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
Plant camouflage provides a novel testing ground for key questions in ecology and evolution.
1 Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, 650201, Kunming, Yunnan, China 2 Centre for Ecology and Conservation, College of Life and Environmental Sciences, University of Exeter, Penryn Campus, Penryn, Cornwall, TR10 9FE, UK
*Correspondence: [email protected] (H. Sun) and [email protected] (M. Stevens).
https://doi.org/10.1016/j.tree.2018.05.010 © 2018 Elsevier Ltd. All rights reserved.
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mistletoes to their host plants has also long been regarded as an adaptation to avoid herbivores [12]. In 1978, Wiens collated many putative examples of resemblance to dead grass, sticks, or stones under the term mimicry [13], although many of these examples should now be regarded as masquerade [8] (see below). More potential cases have been added by Lev-Yadun, as well as other potential defensive functions of coloration [8]. However, work on plant camouflage has been almost entirely descriptive, until more rigorous studies in the past few years have combined techniques in colour measurement [14,15] and knowledge of animal colour vision [16,17] with experimental evidence (see below). It is now clear that several camouflage strategies used by animals apply to plants, with similar key ecological and evolutionary processes and their implications.
A Framework for Understanding Camouflage: Animal Concepts Applied to Plants Here, we outline the main strategies of camouflage that have been identified (for definitions and examples, see Box 1) and discuss comparable cases in both animals and plants (Figure 1; Table S1 in the supplemental information online). These include various types of crypsis to prevent detection and masquerade to hinder recognition and/or classification, plus strategies such as using materials from the environment in decoration [10]. Several strategies for crypsis exist, including matching the background, using disruptive coloration to destroy key body edges and features, and countershading to hide shadows,
Box 1. Key Camouflage Strategies and How They Work For examples of the use of these strategies in animals and putative cases in plants, see Table S1 in the supplemental information online. Background matching works when the bearer generally matches the colour, lightness, and pattern of one (specialist) or several (compromise) background types [10,71]. Disruptive coloration involves a set of markings that create the appearance of false edges and boundaries and hinder the detection or recognition of an object’s, or part of an object’s, true outline and shape [10,72]. Self-shadow concealment and obliterative shading are strategies where directional light, which would lead to the creation of shadows, is cancelled out by countershading [10,73,74] and where countershading leads to the obliteration of 3D form [10]. Distractive markings direct the ‘attention’ or gaze of the receiver from traits that would give away the animal (such as the outline), or interfere with visual mechanisms that an observer could use to detect or recognise an object by virtue of the distractive markings’ high-contrast or conspicuousness [75]. This strategy is controversial [75,76]. Masquerade is a strategy where recognition is prevented by resembling an uninteresting object, such as a leaf or a stick [10], and a masquerading species as one whose appearance causes its predators or prey to misclassify it as a specific object found in the environment, causing the observer to change its behaviour in a way that enhances the survival of the masquerader [77]. Therefore, it is different from forms of crypsis that prevent detection in the first instance. Note that masquerade shares similarities with some other defences, including Batesian mimicry, but they are generally treated as distinct strategies in mechanism and implications. Batesian mimicry involves a mimic resembling a potentially harmful model organism that a predator would normally avoid (such as a hoverfly resembling a wasp). Masquerade, however, involves matching a model that is not normally of interest to the predator, such as a non-living inanimate object such as a stone, or a background object such as a twig. As a consequence, Batesian mimicry might increase the attack rate of a predator on the model species, while masquerade does not. Decoration relates to an organism that (by means of specialist behaviour and/or morphology that has been favoured by selection for that purpose) accumulates and retains environmental material that becomes attached to the exterior of the decorator [30].
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Plant
(A)
(B)
(C)
(D)
(E) No known analogue
(F) No known analogue
(G)
(H)
(I)
(J)
Figure 1. Key Camouflage Strategies in Animals and Plants. (A, B) A juvenile horned ghost crab (Ocypode ceratophthalma, A) and an alpine Corydalis plant (Corydalis benecincta, B) use background matching to blend with the background. (C,D) Juvenile shore crab (Carcinus maenas, C) and seeds of cowpea (Vigna unguiculata, D) can use disruptive colours to hinder the detection of true outline. (E) Eyed hawk moth caterpillar (Smerinthus ocellata, E) has body colours that cancel out the shadows created by directional light (no analogous example has yet been proposed in plants). (F) The white comma mark on the hind wing of comma butterfly (Polygonia c-album, F) has been suggested to be a distractive mark that directs the attention of the receiver from the body outline (no analogue has been proposed in plants yet). (G,H) Young caterpillars of swallowtail butterfly (Papilio sp., G) resemble bird droppings as an example of masquerade, and the living stone plant (Lithops terricolor, H) is widely suggested as a masquerader. (I,J) The long-legged spider crab (Macropodia rostrata, I) decorates itself with seaweeds, and a potential analogue in plants are some coastal plants, passively decorated by sand (e.g., seedlings of Silene sp., J), decreasing their conspicuousness. Photo credits: (A, C, E, G, I) Martin Stevens, (B) Yang Niu, (D) Lian-Yi Li, (F) Jiong-Ao Yang, (H) Keith Green, (J) Simcha Lev-Yadun. See also Table S1 in the supplemental information online.
DecoraƟon
Masquerade
DistracƟve mark
Countershading
DisrupƟon
Background matching
Animal
plus other more debatable concepts (Box 1; Figure 1). Many of these strategies are likely used by plants, too (Table S1). Matching the colour of natural habitats (e.g., leaf litter, bare or rocky ground) is likely in various adult plants [18–20] (Figure 1B), juveniles [21–24], and seeds [25–27] (and even flowers and fruits [28,29]). For disruptive coloration, many seeds have high-contrast spots and stripes that subjectively destroy their outline [8] (Figure 1D). Furthermore, many animals decorate themselves for concealment with objects from their environment [30], and although plants cannot do this actively, some are suggested to obtain a cryptic appearance through passively acquiring decoration materials in certain environments. For example, some coastal and dune plants become covered by sand grains because of their sticky glandular trichomes, thereby making them less conspicuous [31].
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Masquerade acts to prevent recognition, rather than detection, by resembling unimportant objects in the environment that a predator would normally ignore [30]. Analogous to caterpillars matching dead twigs, living stones [32], cacti [13], passion vines [33], mistletoes [34], and certain other cases provide putative examples of masquerade in plants [35] (Table S1), although sometimes the distinction with mimicry and background matching can be complex. Otherwise, across animals there seems to be a greater range of camouflage types than likely occurs in plants, but it is unclear whether this is because they incur fewer constraints (see below), or because much diversity of camouflage in plants is still undiscovered (see [8]).
Current Evidence for Camouflage in Plants While subjective evidence for plant camouflage is often compelling, experimental testing and objective studies are required. A premise that plant camouflage occurs is that visual cues are an important sensory mechanism used by putative enemies (usually insects). Studies often take this as self-evident, but it is important to pay close attention to the natural history of the study system and consider alternative mechanisms, such as olfaction [36]. However, under this premise, first, plant targets should be hard to detect or recognise by antagonists, rather than by humans; and second, plants should obtain higher net fitness through camouflage. Otherwise, since plant coloration might have alternative functions (Box 2), experiments that dissect different (often nonexclusive) hypotheses are needed. Are Plants Camouflaged to Relevant Observers? Vision varies greatly among species, so assessing camouflage requires methods that account for receiver perception [15]. Using advances in measurement technology and knowledge of animal vision, recent studies have verified that plants can be concealed. Approaches have involved either simple comparison of reflectance spectra of plants and the background [18,23,24] or advanced colour vision discrimination models [19–22]. For example, the reflectance of cryptic-coloured bracts of Monotropis odorata is very similar to that of the surrounding leaf litter [18]. In addition, colour information from calibrated images has been used to test the similarity between leaves [24] and seeds [27] with soil substrates. While objective quantification is useful, where possible it is often preferable to consider the vision of the receiver. A specific animal colour vision model (of a herbivorous bird) was first used to verify the resemblance between juvenile leaves of two New Zealand plants (Pseudopanax carssifolius and Elaeocarpus hookerianus) and the leaf litter surroundings [21,22]. A butterfly vision model was also used to quantify colour similarity between two alpine Corydalis plants and their rock backgrounds [19,20]. However, the parameters for these models are often only available for a limited number of animal species, and some plants are consumed by several herbivore groups [24], making it difficult to always use a specific model. So far, most work on plant camouflage has clearly focussed on background matching, regarding colour similarity to substrates. Studies of other types of camouflage, most notably masquerade and disruptive coloration, are very rare. Beyond colour, the leaves of many plants also appear to resemble the size and shape of elements in the environment [37], affording potential masquerade, but quantitative examination is rare. Given that various methods have been developed in animals to quantify visual appearance (e.g., [14,38–40]), further studies on plant camouflage can utilise such approaches. Furthermore, manipulative experiments and tests of receiver detection rates are needed to demonstrate camouflage unequivocally (see below).
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Box 2. Anthocyanin and Camouflage Colour in Plants Anthocyanin is the most important pigment class that contributes to non-green plant colours, including not only bright flowers and fruits but also cryptic seeds and leaves [78]. Different content and types of anthocyanin, and their combination with other pigments (e.g., chlorophyll) and optical structures, can produce various camouflaged colours ([19,20]; Figure IA,B). The accumulation of anthocyanin can be induced by abiotic environment stress, such as strong light, drought, soil salinity, or phosphorus deficiency, and thus might have potential physiological functions in addition to the ecological functions [53]. The light-screening (photoprotection) hypothesis has received most attention recently, according to which anthocyanins can relieve photo-oxidative stress by protecting leaf tissues from harmful effects of light at low temperatures and under other conditions [9,53,79]. This hypothesis can be tested in camouflaged plants by comparing the physiological parameters between different pigment morphs in some polymorphic systems [19]. Nevertheless, such an explanation is not sufficient to explain why some non-photosynthetic organs, for example, seeds and flowers, are also apparently camouflaged due to anthocyanin accumulation. In addition, the accumulation of anthocyanin may accompany increasing chemical defence because they share some common metabolic pathways [80]. Therefore, it is possible that some apparent camouflage colours instead or additionally reflect anthocyanin accumulation accompanied by increasing chemical defence. This explanation is not difficult to test by analysing the actual relationship between these two aspects in camouflaged plants. However, we note that not all camouflage colours involve anthocyanin pigments (Figure IC, D).
(A)
(B)
(C)
(D)
Figure I. Many Camouflaged Leaf Colours, Such as Those in Corydalis hemidicentra (A), Are Formed by Anthocyanins Combined with Other Pigments (e.g., Chlorophyll (B). Plant camouflage can also be achieved without anthocyanin, for example, the scarious bracts of Monotropsis odorata (C) and the silky-lanate hairs covering Saussurea medusa (D). Picture credits: (A, B, D) Yang Niu, (C) Jim Fowler.
Do Plants Obtain Higher Fitness through Camouflage? Higher fitness via concealment might arise from reduced damage rates and higher survivorship and reproductive success. However, it is challenging to examine these advantages in the field for at least two reasons. First, current phenotype may be a result of selection history, with the key enemies now absent [21,22]. Second, it can be difficult to set a proper control, as any artificial changes in colour might introduce unwanted confounds (e.g., changed growth or smell). Nevertheless, some studies have addressed this issue. Using various coloured pine (Pinus sylvestris) seeds combined with natural substrates of different colours, work has shown that seeds with colours that better matched the substrate had lower predation risk from birds [26]. In a more recent study, Strauss and Cacho [24] artificially changed the substrate of cryptic plants of Streptanthus breweri, making them more conspicuous to potential herbivores, which increased damage compared with control plants. This is a clever treatment that increased mismatching without changing the plant itself, but the authors acknowledged that this could change thermal conditions and influence herbivore behaviour [24]. Taking advantage of leaf colour dimorphism in Corydalis benecincta, Niu et al. [19] found that the more camouflaged morph had higher survivorship than a green
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morph in two of three populations studied. While natural dimorphism provides an ideal comparison in this system, more experiments are needed to exclude the potential effect of chemical differences that relate to leaf colour. Other Evidence: Divergence and Convergence In general, patterns of divergence and convergence can provide further evidence of the evolution of plant camouflage. First, because the efficacy of camouflage is environment specific, we expect divergence in camouflage between allopatric populations. Multiple mechanisms can be involved here, depending on the specific species, including genetic adaptation or colour change over various timescales, as well as ontogenetic changes in appearance linked with changes in life history. In animals, there are many examples of differences in camouflage appearance between populations driven by genetic adaptation, such as in mice [41] and lizards [42]. The degree of association can be mediated by levels of migration and gene flow [42]. In species capable of colour change, individuals from the same genetic population can adopt appearances linked to the environment where they settle or develop (e.g., sand fleas [43] and crabs [44]). Some animals also undergo ontogenetic changes linked to differences in habitat use and predator risk [45]. In plants, a significant divergence of seed camouflage colour was reported in a bean (Acmispon wrangelianus) in California between two soil types, namely, serpentine and nonserpentine, and even between sites within the same soil type but of different colour [27]. Given that gene flow is likely because of close distances between sites, this divergence implied strong natural selection on seed colour [27]. More recently, divergence in camouflage leaf colour was found between populations with different rock colours in Corydalis hemidicentra, matching their home background better than others [20] (Figure 2). In contrast to the seed example, this divergence could be consolidated by the isolated habitats produced by the mountainous landscape [20,46]. A similar pattern was also found in leaf colours of S. breweri, which are closer to their home substrates than to other substrates [24], although this was not highlighted by the authors as an adaptive divergence. We also note that there is great intraspecific colour variation between populations of the living stone (genus Lithops), which is thought to be associated with local matches between plants and substrates [47]. These specific local camouflage effects (through background matching) across populations are difficult to explain by alternative nonadaptive hypotheses. In contrast to divergence, unrelated species converge on similar form for camouflage when living in the same visual environment. Numerous animals show similarities in appearance associated with habitat, including, for example, rodents [48] and lizards [42]. Most studied
(A)
(B)
Figure 2. Convergence and Divergence in Plant Camouflage. (A) Convergence in camouflage colour between Fritillaria delavayi (Liliaceae, top) and Saussurea quercifolia (Asteraceae, bottom) in alpine screes (with limestone substrate) from Southwest China. (B) Divergence in camouflage leaf colour among populations of Corydalis hemidicentra. Picture credits: (A) Hang Sun, (B) Yang Niu.
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cases are due to genetic mechanisms [48,49], but similarities could equally arise in different species of organism that are all capable of plasticity (e.g., crustaceans). In plants, a brief survey of the local flora of New Zealand and North America found descriptive evidence of convergent plant colours that match the substrates [50]. A similar convergence has also been found in the alpine plants of Southwest China (Figure 2; see [19]). Furthermore, many plants in sandy environments are suggested to have similar pale colours through different mechanisms [31]. However, no rigorous tests have yet been conducted to examine these phenomena.
What Factors Constrain or Promote the Evolution of Plant Camouflage? Costs and Constraints on Plant Camouflage Evolution Compared with animals, cases of camouflaged plants are seemingly less common, and the types of camouflage strategies are also apparently less diverse. This might be because until recently, plant camouflage had not been studied regularly, or it could be due to intrinsic differences between plants and animals. Camouflage incurs inevitable physiological and ecological costs in animals [5], but costs and constraints might be more considerable in plants (especially for their shoots). At least three general classes of limitation, that is, in physiology, camouflage efficacy, and selection strength, might hinder the evolution of plant camouflage (Table S1). Different from many animals, most plants are autotrophic and have to be green (the colour of chlorophyll) to live via photosynthesis. This is likely to be one reason why certain camouflage strategies used by animals, such as transparency, have not been found in land plants. Furthermore, any non-photosynthetic pigment might decrease photosynthetic performance [51,52] and thereby influence the fitness of the whole plant. For example, in a number of redleaved plants there seem to be costs of being non-green in photosynthesis [52–54]. In colourdimorphic C. benecincta, however, the rock-like morph and the green morph share similar photosynthetic performance [19]. Possibly due to restrictions on finding suitable study systems, work addressing potential costs and constraints is still rare and needs further attention. Plants cannot escape in most of their life stages and therefore can be located and attacked by enemies repeatedly. For the same reason, enemies can learn to detect or recognize them (as also suggested by Williamson [55]). In addition, plants cannot choose microhabitats that optimize their camouflage actively, as some animals do [56], which can improve camouflage. In turn, most flowering plants need to attract pollinators for reproduction, and their flowers may inevitably decrease camouflage efficacy. However, these arguments are not entirely convincing because many animals also use conspicuous sexual signals, and one can argue that because plants cannot escape, their need for camouflage should be greater, not lower. A majority of plants are modular organisms composed of numerous similar structures (e.g., leaves and flowers), which is not the case for many animals. Given this, many mature plant individuals can be more robust (to tolerate and survive attack and regrow), such that selection might be not as strong as it is in animals to induce any fitness advantage conferred by camouflage. Differences in structure between plants and animals might also influence their general appearance, potentially another reason why some camouflage strategies, such as countershading, have not been found in plants. Factors That May Facilitate Plant Camouflage Evolution Camouflage will have higher opportunity to evolve when the above-mentioned constraints are weak or broken, such as in plants that do not rely on photosynthesis. Monotropis odorata [18] (see Figure IC in Box 2) and other heterotrophic plants [57] are potential examples. The specific Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
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life stage of a plant, such as its seeds (when photosynthesis is not necessary), might also provide better candidates to expect camouflage. To break the latter two constraints (low camouflage efficacy and low selection strength), specific habitats and sizes (or ages) of plants might be favoured. An open habitat not only increases the pressure of visual selection [20,50,58] but also facilitates better camouflage by providing no landmarks for enemies to locate targets. Each individual can also incur a higher risk of damage (stronger selection strength) in such habitat due to low plant density. In addition, small plants could obtain better camouflage for two reasons. First, they are inconspicuous per se compared with larger plants. Second, backgrounds are often more diversified at smaller size scales, providing complex visual environments that are known to facilitate camouflage [59]. Meanwhile, selection on small plants should be stronger because they are more fragile. Consistent with this idea, camouflage has often been found in either small herbs [18–20,24] or the fragile stages of plant life history, such as juveniles [21–23] and seeds [25–27]. This again parallels many animal systems, where juveniles are often apparently more concealed than adults. Overall, stronger selection has been shown to facilitate the evolution of camouflage in plants. For example, cryptic-coloured plant species were found to suffer seven times more damage than the normal green species in some flora [50]. Improved camouflage efficacy was found to associate with higher damage risk among populations of C. hemidicentra [20]. Furthermore, specialized enemies might impose stronger selection compared with generalists, since they can overcome or even utilise the plant’s chemical defences [60], forcing hosts to evolve alternative defensive strategies. For example, butterfly specialists are suggested to be the main selective agent in several camouflaged plant genera, including Corydalis (Apollo butterflies [19,20]), Streptanthus (pierid butterflies [24,26]), and Passiflora (Heliconius butterflies [33]). It is interesting to note that mistletoes, a resemblance system that still attracts debate [61,62], are also important host plants of some butterflies [34], which have been neglected as a potential selection pressure for a long time [63]. Collectively, current evidence suggests that heterotrophism, open habitats, small individual size, fragile structure, and specialized enemies might facilitate the evolution of plant camouflage.
Other Key Ecological and Evolutionary Issues Regarding Plant Camouflage Evolutionary Consequences of Camouflage Camouflage can place considerable selection pressure on enemies, which can often manifest as changes in enemy search behaviour or perceptual mechanisms. In animals, predators are thought to adopt search images for camouflaged prey [64], involving heightened attention toward recently encountered or common prey. A key outcome can be negative frequencydependent (apostatic) selection [65], whereby common morphs are found disproportionately often compared to rarer morphs, leading to a selective advantage of rare forms. This can favour prey polymorphism and fluctuations in morph frequency over time. Overall, many animals are polymorphic, and this has been studied in snails [66], moths [67], and other organisms both in the context of matching different backgrounds and apostatic selection. Other work has demonstrated how search images occur in predators and link to diversity in prey appearance in computer experiments [65]. Studying search images and the reasons for polymorphism in the wild is notoriously difficult, however. In plants, it is entirely possible that these processes occur and lead to polymorphism in camouflage appearance (see the dimorphic leaf colour in C. benecincta [19]). The work of Nystrand and Granstrom [26] found 8
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that bird predation can drive or maintain colour dimorphism in seed camouflage, possibly through search image mechanisms. In contrast to search images and apostatic selection, intraspecific diversity may arise if selection favours individuals that match different patches in the same location. Across populations, specific local matching can hinder migration between populations because of potentially higher mortality induced by mismatching intermediate forms. This process can decrease gene flow between populations and thus consolidate divergence in colour and other characters. It could even promote speciation, as indicated in some animals, for example, stick insects [68]. Alternatively, a compromise or generalist camouflage can arise and allow migration between habitats with different colours. When individuals are potentially seen in multiple visual environments or patches of different appearance, individuals may utilise an intermediate or generalist appearance between multiple background types while matching none perfectly. Some experiments in artificial systems show that compromise camouflage could work (e.g., [69]), but this has not yet been demonstrated in real animals. In plants, this strategy has been implied in C. hemidicentra, where camouflage is not so specialist but apparently resembles several backgrounds [20]. Compromise camouflage could also occur in the dispersal stages (e.g., seeds), when they might face different habitats or backgrounds. In general, much theory has been developed regarding the evolution of specialist versus generalist camouflage strategies in mobile animals, and it will be important explore these ideas in plants. Potential Influence of Human Activity on the Evolution of Plant Camouflage Humans have a major influence on the natural world, and this includes several examples of camouflage (e.g., industrial melanism and the peppered moth [67] and climate change and snowshoe hares [70]). In plants, commercial harvesting could be a major selection pressure. For instance, commercial harvests in the Himalayas are suggested to explain the dwarfing process of Saussurea laniceps in the past 100 years. We have recently noticed that the putative camouflage of the traditional medicinal plant Fritillaria delavayi may correlate with the strength of selection by commercial harvests in Southwest China and neighbouring regions. A similar process might also be happening in South Africa on living stones, which have suffered heavily from commercial collection [32]. Given rapid human-induced changes, it is valuable to test whether and how human activities influence the evolution of camouflage in these plants, and their consequences.
Concluding Remarks It has long been known that colour is important in the communication between flowers and pollinators, and now it is apparent that plants use colour to hide from enemies, too. Camouflage has been documented in a number of plants from different continents, the efficacy and fitness of which have been verified in some cases, with the evolutionary process either illustrated or implied. Although studies are still limited, there are noticeable factors that facilitate the evolution of plant camouflage. However, we are at the beginning of this field, and more experimental studies are needed to uncover generalities and to answer many unsolved questions (see Outstanding Questions). Nevertheless, there is a wealth of theory and concepts from animal camouflage to utilise, where the evolution, mechanisms, and efficacy of camouflage are attracting the attention of evolutionary biologists, behavioural biologists, psychologists, vision scientists, and others. The emerging picture of plant appearance is that plants do far more than entice pollinators and photosynthesise with their colours, but we now need to discover just how important a role camouflage has in their ecology and evolution, and to their enemies.
Outstanding Questions What mechanisms enable plant camouflage? Camouflage form can stem from genetic mechanisms or from phenotypic plasticity. The specific mechanism, and its flexibility, can have a major influence on the nature of camouflage and its implications, and how organisms respond to spatial and temporal uncertainty [81]. Reciprocal transplantation and common garden experiments will be valuable to test the relative importance of these two mechanisms in plants. Is there a conflict between strategies toward friends versus enemies and how can it be solved? The trade-off in animals between camouflage and sexual signals has been a subject of long-standing study (e.g., [82,83]). This trade-off might also exist in plants that need to attract pollinators as well as avoid enemies. Using different sensory modalities [18] and phenological mismatches [19] between them can be possible solutions. How common is camouflage in plants? Although many putative camouflage cases have been suggested [8,13,37,84], more studies are needed to examine them, especially for strategies other than background matching. Based on these studies, we can estimate the geographic and phylogenetic distribution of plant camouflage and the factors driving plant evolution using comparative studies. How important is camouflage for plants? Plants adopt various defensive strategies. It will be valuable to investigate the relationship between camouflage, other defensive coloration strategies (e.g., aposematism), other non-colour defences (e.g., physical and chemical defences), and when and why different defences evolve. What are the evolutionary consequences of plant camouflage? There is much to learn regarding how phenotypic polymorphism, genetic isolation, and even speciation can be influenced by the evolutionary process of plant camouflage. Could the evolution of plant camouflage be influenced by human selection? Direct commercial harvesting can be a strong selective pressure on the evolution of wild animals [85], which might also influence the visual characters of
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Acknowledgements We thank Keith Green, Jim Fowler, Simcha Lev-Yadun, Lian-Yi Li, and Jiong-Ao Yang for generously providing images. We thank Tim Caro and Simcha Lev-Yadun for helpful comments on the manuscript. This work was supported by the Strategic Priority Research Program of Chinese Academy of Sciences (XDA 20050203 to H.S.)，Major Program of the NSFC (31590823 to H.S.), the National Key R & D Program of China (2017YF0505200 to H.S.), NSFC (31670214 to Y.N.), Yunnan Applied Basic Research Projects (2016FB035 to Y.N.), and Youth Innovation Promotion Association, CAS (2018427 to Y.N.).
Supplemental Information Supplemental information associated with this article can be found online at https://doi.org/10.1016/j.tree.2018.05.010.
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