Natural enemy ecology: comparing the effects of predation risk, infection risk and disease on host behaviour

Abstract

SummaryGrowing interest in unifying the field of natural enemy ecology has revealed similarities between predation and parasitism. In parallel with predation, parasite infection – and even the threat of infection – can alter host traits and indirectly affect community interactions. Nonetheless, few studies have considered multiple mechanisms of natural enemy‐induced behavioural alteration in parallel (e.g. effects before and after enemy contact) or the factors that drive variation in behavioural responses.We first evaluated how the threat of infection by a virulent trematode (Ribeiroia ondatrae) compared to the well studied risk of predation in triggering inducible defences in amphibian hosts, prior to direct contact with either enemy. We then evaluated five separate factors that influenced the magnitude of parasite‐induced behavioural changes after successful transmission.In both the laboratory and an outdoor mesocosm experiment, we found no evidence that tadpoles of two species (Pseudacris regillaandAnaxyrus boreas) altered their activity levels in response to chemical cues from uninfected host snails, trematode‐infected snails, or from conspecifics actively becoming infected. In contrast, tadpoles sharply reduced their activity in response to lethal predation risks posed by caged dragonfly larvae.After infection, however,Ribeiroiacaused strong decreases in host activity and escape distance that correlated positively with infection intensity and negatively with host size and developmental stage. Five days after infection with a one‐time pulse exposure, hosts recovered to near‐normal activity levels. Hosts exposed to a chronic daily exposure of equal intensity, however, continued to decrease activity. UnlikeRibeiroia, two less virulent trematodes had no detectable effects on host behaviour.Our results highlight key distinctions between predation and parasitism. The contrasting effects prior to enemy contact may stem from the fact that unlike predation, the consequences of macroparasite infection are intensity‐dependent and unpredictable. In contrast, the strong changes in host behaviour after infection are more similar to non‐consumptive predator effects in terms of their potential influences on host fitness and community interactions.