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

Abstract

Summary1. Growing 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. 2. 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. 3. In both the laboratory and an outdoor mesocosm experiment, we found no evidence that tadpoles of two species (Pseudacris regilla and Anaxyrus 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. 4. After infection, however, Ribeiroia caused 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. Unlike Ribeiroia, two less virulent trematodes had no detectable effects on host behaviour. 5. 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.

Parallel and nonparallel behavioural evolution in response to parasitism and predation in Trinidadian guppies

“…Most studies of such effects have focused on predators rather than parasites, perhaps because parasites are less likely to directly cause mortality (Combes, 2001). Yet indirect effects of both forces are also possible, whereby 'fear' of predators reduces fitness (Clinchy et al, 2013) and infection by parasites alters behaviour, reduces fecundity or mating success (Raffel et al, 2008;Preston et al, 2014). Recognizing the existence of such effects, and the fact that parasites tend to be much more abundant than predators, it remains uncertain which class of enemy has a stronger effect on the evolution of natural populations, especially on behavioural traits (Kortet et al, 2010).…”

Experimental investigation of alternative transmission functions: Quantitative evidence for the importance of nonlinear transmission dynamics in host–parasite systems

“…Second, host behavioural traits and responses to infection may contribute. Because parasites such as R. ondatrae cause considerable damage to the host tissue during encystment, often leading individuals with heavy infections to exhibit reduced activity 12–48 hr following exposure, shifts in host behavioural responses (including reduced avoidance behaviour) could enhance transmission in a nonlinear manner—particularly if it generated among‐host variation (Johnson & Hoverman, ; Preston, Boland, Hoverman, & Johnson, ). Other studies have reported that variation in host size or developmental stage can also influence parasite aggregation (Holland et al., ), although we endeavoured to keep these traits as constant as possible within our manipulations.…”

Asymmetric competition shapes amphibian response to rapid environmental change

“…We tested the interplay between biotic and abiotic constraints on amphibian response to climate change, as these animals are sensitive to environmental stress and have long been used to investigate antagonistic interactions, particularly competition, predation, and parasite/pathogen dynamics (e.g., Peacor and Werner , Preston et al. , Youngquist et al. ).…”

“…This complex interplay requires evaluation of how changing environmental conditions affect the strength and direction of multi-species interactions (e.g., Hoover et al 2012, Milazzo et al 2013, Rysavy et al 2016) and, potentially, how interactions can mediate the impact of environmental stress (e.g., McGuire and Agrawal 2005, Suttle et al 2007, Alexander et al 2015. We tested the interplay between biotic and abiotic constraints on amphibian response to climate change, as these animals are sensitive to environmental stress and have long been used to investigate antagonistic interactions, particularly competition, predation, and parasite/pathogen dynamics (e.g., Peacor and Werner 1997, Preston et al 2014, Youngquist et al 2015. While pairwise assessments of species interactions under different environmental conditions are quite valuable (see Rogers andChalcraft 2008, Vogel andPechmann 2010; for further review of amphibian experiments see Appendix S1: Tables S1 and S2), we posit the need for research investigating the combined effects of multiple interacting amphibian species and environmental stress.…”