The legacy of predators: persistence of trait-mediated indirect effects in an intertidal food chain

Trait mediated indirect effects are integral to many multiple-level predator-prey interactions. They arise routinely when, in response to predators, prey decrease their foraging on a basal resource, often due to fear. Less examined is a common assumption about trait-mediated indirect effects: that reductions in prey foraging track the instantaneous presence or absence of predators. In particular, although it is recognized that behavioral, physiological, and morphological changes in prey can persist after a predator departs, whether those changes ultimately affect trophic levels below remains an open question. Here, we tested whether legacy effects of predators lead to trait-mediated indirect effects that persist beyond when predators are present, using a model intertidal system that included a crab predator (Cancer productus), a carnivorous snail prey (Nucella ostrina), and a basal suspension feeder (the mussel, Mytilus californianus). We found that previous conditioning of snails to predator cue instilled a sustained behavioral fear response that depressed foraging by snails for at least two weeks beyond when the predator cue was present. Indeed, snails conditioned previously to predator cue consumed similar numbers of mussels as snails currently subjected to cue. Because such durations are long enough to allow new mobile predators to enter prey detection domains previously vacated by other predators, these findings suggest that neglecting the time course of persistence of trait-mediated indirect effects could appreciably underestimate their strengths. Our study supports the notion that prey use prior experience in addition to their body state to inform their anti-predatory decision making, which results in a persistent trophic cascade.