Trait-Mediated Effects in Rocky Intertidal Food Chains: Predator Risk Cues Alter Prey Feeding Rates

The influence of predation on rocky intertidal community structure has long emphasized the importance of indirect interactions. Most efforts in this area have focused on the density-mediated, or lethal effects, of predators on prey density. Recently, there has been growing interest in trait-mediated indirect interactions (TMIIs): the presence of a predator in the environment influences the interaction between two other species (prey and their resource) by altering a trait of the prey species. For example, waterborne cues released by predators can cause changes in prey species behavior, such as feeding rates, thereby altering the impact of the prey species on their resources. Thus, TMIIs represent the nonlethal effects of predators that contrast with the more traditional emphasis on lethal indirect effects. Marine ecologists are just beginning to explore the role of TMIIs in their systems. We examined whether risk cues released by a ubiquitous crab predator (Carcinus maenas) influence the abundance of two dominant species in the rocky intertidal zone (barnacles [Semibalanus balanoides] and fucoid algae [Ascophyllum nodosum]) by altering the behavior of two of its snail prey (Nucella lapillus and Littorina littorea). We found that the presence of green crab risk cues can have strong cascading indirect effects on the abundance of barnacles and fucoid algae. N. lapillus exposed to risk cues consumed up to 29% fewer barnacles compared to conspecifics feeding in the absence of risk cues, whereas L. littorea exposed to risk cues consumed 459% fewer fucoids compared to conspecifics feeding in the absence of risk cues. These cascading interactions appear to reflect suppression of snail feeding by predator risk cues. In both food chains, snails exhibited more refuge-seeking behavior and grew less in the presence of risk cues. Our experiments suggest that TMIIs may have an important and underappreciated influence on species interactions that shape community dynamics on rocky intertidal shores.