Seasonal plasticity for anti-predatory strategies: matching colour and colour preference for effective crypsis

Abstract

Effective anti-predatory strategies typically require matching appearance and behavior in prey, and there are many compelling examples of behavioral repertoires that enhance the effectiveness of morphological defenses. When protective adult morphology is induced by developmental environmental conditions predictive of future predation risk, adult behavior should be adjusted accordingly to maximize predator avoidance. While behavior is typically strongly affected by the adult environment, developmental plasticity in adult behavior -- mediated by the same pre-adult environmental cues that affect morphology -- could ensure an effective match between anti-predatory morphology and behavior. The coordination of environmentally-induced responses may be especially important in populations exposed to predictable environmental fluctuations (e.g. seasonality). Here, we studied early and late life environmental effects on a suite of traits expected to work together for effective crypsis. We focused on wing color and background color preference in Bicyclus anynana, a model of developmental plasticity that relies on crypsis as a seasonal strategy for predator avoidance. Using a full-factorial design, we disentangled effects of developmental and adult ambient temperature on both appearance and behavior. We showed that developmental conditions affect both adult color and color preference, with temperatures that simulate natural dry season conditions leading to browner butterflies with a perching preference for brown backgrounds. This effect was stronger in females, especially when butterflies were tested at lower ambient temperatures. In contrast to the expectation that motionlessness enhances crypsis, we found no support for our hypothesis that the browner dry-season butterflies would be less active. We argue that the integration of developmental plasticity for morphological and behavioral traits might improve the effectiveness of seasonal anti-predatory strategies. IMPACT SUMMARY To avoid predation, prey rely on strategies that typically include a variety of morphological and behavioral characteristics working together to deceive or scare predators. While some protective traits are a constitutive property of the prey species (e.g. hedgehog spines), others are produced only when the risk of encountering predators is high. For example, Daphnia crustaceans develop protective helmets and spines when exposed to cues that signal predator presence. When anti-predator morphologies are environmentally-induced, or plastic, the responses of associated behavioral traits should also be environmentally-dependent to ensure that animals exhibit behavioral repertoires that match their appearance. We used the tropical butterfly Bicyclus anynana, the squinting bush brown, to study these coordinated responses. In its natural habitat, with alternating dry and wet seasons, this thermally plastic butterfly alternates between seasonal forms with distinct wing color patterns related to distinct strategies to avoid predation. Dry season individuals, which develop under cooler temperatures, have small pattern elements on their wings and are cryptic against the brown background of dry foliage. In contrast, wet season individuals have large ornamental pattern elements that deflect attacks from predators towards the wing margin and away from their vulnerable bodies. We tested whether the cooler temperatures of the dry season also influenced other traits that can presumably improve the effectiveness of camouflage. In particular, we found that both the ornamental colors (appearance) and the choice of resting background colors (behavior) were affected by the temperature experienced during development. We found that dry season temperatures lead to browner butterflies with a stronger preference to rest on brown backgrounds. While behavior is typically very flexible in relation to changes in the adult environment, a developmental imprint on adult behavior can help ensure an effective match between the cryptic appearance and background choice behavior.