Alpine scree plants benefit from cryptic coloration with limited cost

Abstract

Like animals, plants are attacked by enemies (herbivores) that forage using visual cues; however, the defensive coloration type known as cryptic coloration was rarely reported in plants. For most autotrophic plants, because photosynthesis relies on the presence of chlorophyll, a green leaf appearance is standard. However, if having leaves that are not green is more beneficial than costly, such coloration may evolve under certain conditions. Taking advantage of the leaf color dimorphism of Corydalis benecincta, we showed that the cryptically colored leaves confer a clear benefit without obvious cost in natural populations. Based on this study, we try to provide a framework on which to base a cost–benefit analysis to investigate the evolution of cryptic leaf coloration in plants.

Crypsis via coloration is a common defensive strategy in animals, but was given much less attention in plants,¹ even though plants are also attacked by various enemies that rely on visual cues when foraging. In the last years, increasing evidence from experimental studies has demonstrated that plants also use crypsis to avoid attacks by herbivores.^2-5 However, a universal framework to understand the evolution of this character has not been applied effectively in plants (see the suggestion by Burns⁶).

As pointed out by Burns,⁶ experimental tests of the hypothesis that a plant is cryptically colored are difficult because an appropriate control cannot be easily designed by manipulating the plants’ color (but see Strauss et al.² for an alternate method). This may be the reason why experimental studies to investigate this hypothesis are so limited. In a recent study, we used Corydalis benecincta W. W. Smith (Papaveraceae), an autotrophic alpine scree plant with dimorphic leaf color (either green or gray, the latter strongly resembling the scree background), to investigate whether leaf color serves as defense.⁷

Although organisms may benefit from defensive coloration, many times it also incurs inevitable costs.⁸ For plants, this can be because: 1) extra compounds may be required to maintain the cryptic coloration, 2) such non-photosynthetic pigments may reduce photosynthetic efficiency by absorbing visible radiation or/and competing with photopigments over photon capture, and 3) the inconspicuous coloration may reduce their visual attractiveness to flower or fruit visitors, resulting in reduced mating and dispersal opportunities⁷ (Fig. 1). It is reasonable to expect that cryptic coloration would evolve only when it provides more benefits than costs.

Figure 1. A primary framework for studying the evolution of cryptic coloration in plants based on a cost–benefit analysis.

Following the advice of Burns,⁶ we first showed that in the herbivores’ (in this case a butterfly) color vision model it is difficult to locate the gray morphs that strongly resemble to the scree background, corroborating the premise that this coloration is cryptic in the eyes of relevant herbivores. We then showed that the cryptic coloration provides clear benefits (lower damage and higher survivorship) with limited costs in anthocyanin synthesis (which contributes to forming the gray color) and no obvious cost in photosynthetic performance and visual attractiveness to flower visitors.⁷

Although leaf color does not always influence photosynthetic performance, non-green leaves of some species, such as Prunus cerasifera,⁹ Cistus creticus,¹⁰ and some cultivars with leaf variegation,¹¹ have been found to perform less well than the green ones. Taking advantage of the natural leaf color dimorphism of Corydalis benicincta, we confirmed that the plants with cryptic coloration incurred no cost in photosynthetic performance, although they differ in their pigment composition from the green morph.⁷

For animal-pollinated autotrophic plants, a potential cost may also result from the conflicting requirements of survival (being inconspicuous to herbivores) and reproduction (being conspicuous to pollinators). We did not find that the gray morphs were less attractive to flower visitors than the green ones, possibly because both of them have flowers with the same bright color. However, such flowering may impede the evolution of cryptic coloration, as bright colors may also be obvious to herbivores. One possible explanation that may resolve this conflict is that there is a time mismatch between oviposition and flowering (personal observation, Fig. 2). This scenario has been reported in another system, namely between Parnassius and Corydalis species.¹² Therefore, it is reasonable to presume that individuals with cryptic coloration may take advantage of this trait before the flowering season (during the ovipositing period in our case). Another possibility is that ovipositing butterflies may avoid flowering plants as flowers may cue that the leaves are old or less nutritious but chose young individuals as host plants (observed by Kai Li and Bin Cheng in other Parnassius–Corydalis systems, personal communication). Many Parnassius butterflies (e.g., P. cephalus Figure 3) lay their eggs on the rocks near the food plant rather than on the plant itself.¹³ It has been hypothesized that this behavior confers an adaptive advantage if the egg does not hatch in the first year, because it will remain in situ rather than being attached to a withered plant part that could blow away.¹² Indeed, young plants may represent a more reliable food resource for offspring than the flowering plants, as the latter are less likely to survive until the next year (especially if they are perennial monocarpic plants). Both of these scenarios could facilitate the evolution of cryptic coloration as it provides defensive benefits at the pre-flowering stage in the life cycle of the plant. To examine this question, we are investigating the life history of this system, currently very poorly studied, in more detail.

Figure 2. The eggs of Parnassius near by the host plant Corydalis benecincta with green leaves before flowering.

Figure 3. Adult of Parnassius cephalus, one of the herbivores of Corydalis benecincta.

The various Corydalis species and the diversity of habitats in SW China provide clues to help us understand the evolution of cryptic leaf coloration: both specialized habitats and the stress from herbivores are crucial for the evolution of cryptic coloration.⁷ Using the results of a molecular phylogeny study of Corydalis in China,¹⁴ we found that species with gray leaves have evolved several times from the ancestral green condition, exclusively in the alpine scree habitat. Interestingly, several scree plants from New Zealand, such as Notothlaspi rosulatum, also have a leaf color that strongly resembles their rock habitat when they are young, low and very succeptible.⁶ The extreme environmental conditions associated with alpine scree may induce the production of anthocyanins,^15,16 which contribute to form this leaf color. In addition, plants may suffer higher stress from herbivores in such habitats with open vegetation.² In our study, we noted that the gray leaf color had not evolved in the alpine meadow species nor in a scree congener that did not suffer obvious herbivore damage (see Fadzly et al.⁵ for similar results based on the historical distribution of currently extinct herbivores). These results allow us to consider that, for plants growing in a “normal” habitat (e.g., meadow), the green color may be inconspicuous (see Lev-Yadun and Ne’eman¹⁷ for the reverse scenario). A phenomenon that may support this suggestion is that ovipositing butterflies do not always land on the right host plant in a community composed of many plant species.¹²

Niu Y, Chen G, Peng D-L, Song B, Yang Y, Li Z-M, Sun H. Grey leaves in an alpine plant: a cryptic colouration to avoid attack? New Phytol. 2014;203:953–63. doi: 10.1111/nph.12834.