A role for the local environment in driving species-specific parasitism in a multi-host parasite system

The extent and magnitude of parasitism often vary among closely related host species and across populations within species. Determining the ecological basis for this species and population-level variation in parasitism is critical for understanding infection dynamics in multi-host-parasite systems. To investigate such ecological underpinnings of variation in parasitism, we studied Enallagma damselfly host species and their water mite (Arrenurus spp.) ectoparasites in lakes. We first evaluated how host identity and density could shape parasitism. To test the effects of con- and heterospecific host density on parasitism, we used a field experiment with Enallagma basidens and E. signatum. We found that parasitism did not vary with con- or heterospecific density and was determined by host identity alone, with no spillover effects. We also evaluated the potential role of local adaptation and resource availability in shaping parasitism. To do so, we used E. signatum in a reciprocal transplant experiment crossed with a prey resource-level manipulation. This experiment revealed that parasitism declined sharply for one host population in its non-local lake, but not the other source population, with no effects of prey levels. This asymmetry implies that damselflies express enhanced defences against parasitism that are neither population-specific nor dependent on resource abundance, or that mites developed heightened local host specificity. The results of multivariate modeling from an observational study generally supported these experimental findings: neither host density nor resource abundance strongly explained among-population variation in parasitism. Instead, local abiotic conditions (pH) had the strongest relationship with parasitism, with minimal associations with predator density, temperature and a measure of immune function. Collectively, our findings suggest a crucial role for the local environment in shaping host-parasite interactions within multi-host-parasite systems. More generally, these results show that research at the intersection of community ecology and disease ecology is critical for understanding host-parasite dynamics within natural communities.