Reducing Predation through Chemically Mediated Camouflage: Indirect Effects of Plant Defenses on Herbivores

Herbivores often specialize on particular hosts that provide both food and shelter from natural enemies. It is thus often unclear whether a plant's value as a food or its value as a safe shelter has played a larger role in selecting for specialization. Decorator crabs offer a novel opportunity to investigate the relative effects of diet vs. natural enemies in selecting for specialization because these crabs place plant "shelter" on their backs as camouflage but need not use these plants as food, thus decoupling the plant's value as a food from its value as a shelter. In this study, we show that juveniles of the decorator crab Libinia dubia selectively decorate with the chemically defended brown alga Dictyota menstrualis but treat this plant as a low-preference food. Common omnivorous fishes that are potential predators of Libinia avoid consuming Dictyota due to the alga's potent chemical defenses. In the field, juvenile crabs decorated with Dictyota experience significantly less predation than crabs decorated with an alga that is not chemically noxious to local fishes, and the Dictyota metabolite that most strongly deters feeding by fishes is the specific metabolite that determines decoration choice by this crab. Thus, by behaviorally sequestering defenses from this chemically noxious plant, these small crabs reduce their susceptibility to predation. In the presence of predators, juvenile crabs reduce their rate of feeding, but not of decorating, suggesting that antipredator behavior such as decorating takes precedence over feeding. In addition, only juvenile crabs that are of a size that can be consumed by local fishes decorate at all. Adult crabs that have carapace widths exceeding the gape size of co-occurring fishes do not decorate in either the field or the laboratory. Apparently predation, rather than diet selection, drives decoration specialization in Libinia, highlighting how indirect effects of plant secondary chemistry can impact herbivore behavior, ecology, and evolution.