Trait-mediated indirect effect involving a chain of learning in agroecosystems

An increase in predation risk triggers a trait response of prey, which alters the interactions between the prey and other species, ultimately affecting other species in the ecosystem. Such predator-driven trait-mediated indirect effects (TMIEs) may have been shaped by long-term evolutionary processes involving the organisms involved, but learning may also be important, especially in contemporary ecosystems experiencing repeated biological invasions. The apple snail Pomacea canaliculata is an important introduced pest of rice, Oryza sativa. Recently, the carrion crow Corvus corone has been found to prey on this species only in some areas, suggesting that learning is involved in this predation. In addition, apple snails can learn to escape from predators and exhibit predator-specific responses. Thus, the “chain of learning” by the crow and the snail may shape novel TMIEs in the rice ecosystem. We conducted field and mesocosm experiments to test this hypothesis. In the field experiment, we simulated predation by crows in rice fields and investigated the behavior of apple snails. The snails exhibited escape behaviors in response to the simulated predation, and both the proportion of individuals showing the escape response and the degree of escape response were greater in fields with predation by crows than those without predation. In the mesocosm experiment, apple snails from fields with and without predation by crows were separately introduced into mesocosms simulating rice fields, and the behaviors of the snails and the number of remaining rice plants were recorded for 16 days at three levels of predation risk (daily, every 4 days, or no predation). Both the presence/absence of predation in the collection fields and simulated predation affected the escape responses of the snails. Moreover, damage to rice was more severe in mesocosms containing snails from fields without predation than those containing snails from fields with predation. These results suggest that the “chain of learning” causes TMIEs in agroecosystems.