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

Background/Question/Methods

Animals in nature exist in complex communities in which they must defend against multiple enemies, including parasites and predators. Despite this realization, ecologists have rarely used the same context to study host/parasite and predator/prey interactions. A comprehensive understanding of the similarities and differences between predation and parasitism requires examining the effects of both natural enemies at multiple phases of the interaction (e.g., before and after parasite infection) and an exploration of factors that drive variation in responses. Here, we used laboratory studies and a mesocosm experiment to first evaluate how the threat of infection by virulent trematode parasites (Ribeiroia ondatrae) compared to risks posed by lethal dragonfly predators (Anax junius) in triggering inducible defenses in amphibians, prior to direct contact with either natural enemy. We utilized treatments that allowed us to distinguish possible effects of host snails, trematodes themselves, conspecifics actively becoming infected or dragonfly predators. We then conducted a series of laboratory trials that examined parasite-induced behavioral changes after successful transmission. Our experiments specifically disentangled the roles of parasite identity (three parasite species), infection intensity (six dosages), time-since-exposure (one to five days), exposure duration (pulse vs. chronic), and host developmental stage in driving the magnitude of host behavior changes

Results/Conclusions

Consistent with anti-predator defenses, caged dragonflies elicited reductions in activity and changes in morphology of two tadpole species (Pseudacris regilla and Anaxyrus boreas). Despite this response to predators, we found no evidence that tadpoles exposed to chemical cues from infected snail hosts, Ribeiroia parasites, or conspecifics becoming infected altered their behavior or morphology in response to infection risk. After infection, however, Ribeiroia caused strong decreases in host activity and escape distance that correlated positively with infection intensity and negatively with host size. Five days after infection with a one-time pulse exposure, hosts recovered to near-normal activity levels, whereas hosts exposed to a chronic daily exposure of equal intensity continued to decrease activity. Unlike Ribeiroia, two less virulent trematodes had no detectable effects on host behavior. Our results highlight key distinctions between predation and parasitism. While multiple reasons may underlie the absence of a host response to infection risk, this finding may stem from the fact that consequence of macroparasite infection are intensity-dependent and difficult to predict prior to transmission. In contrast, the strong changes in host behavior after infection are more similar to nonconsumptive predator effects in terms of their potential influences on host fitness and community interactions.