Climate-driven shifts in host-parasite interactions: Consequences for parasite transmission and host pathology.

摘要

Interspecific differences in climate-driven changes to organismal physiology and phenology will alter the timing and consequence of many ecological interactions. The extent to which such changes may exacerbate or ameliorate disease risk is increasingly controversial. I used a combination of laboratory and field studies to simultaneously test both direct (i.e., physiological) and indirect (i.e., interspecific interactions) effects of climate change on disease using the parasite, Ribeiroia ondatrae, and its hosts as a model system. Ribeiroia is transmitted sequentially from snails to amphibians to birds, and when amphibians are infected early in development, they are more likely to die or become deformed. Because parasite development is enhanced by elevated temperatures while amphibian breeding is jointly constrained by temperature and rainfall, I hypothesized that climate change could lead to greater infection of tadpoles at earlier stages of development, causing elevated pathology. By infecting snails at different temperatures in the laboratory, I found that higher temperatures accelerated parasite development and amplified snail pathology (via reduced egg output), but also decreased snail survival time. Similarly, in amphibians, parasite infectivity (host penetration) was enhanced, but establishment (encystment), persistence, and survival outside the host declined with rising temperature. There was a mid-temperature peak in deformities, likely resulting from increases in parasite infectivity with temperature coupled with reductions in host vulnerability owing to faster development. My field survey revealed a negative association between evaporation and the density of infected snails as well as amphibian infection intensity (independently of the snail effect), likely due to reduced host and parasite survival and production at sites subjected to drying. After accounting for Ribeiroia infection intensity, amphibian deformities were also positively correlated with nutrients, suggesting a potential effect of eutrophication on host tolerance or parasite virulence. Different aspects of climate change will thus act to enhance infection in some ways, but hinder it in others, suggesting that future research into climate-disease interactions should use a combination of field and laboratory studies that focus on potential nonlinearities between climate and disease risk, shifting host-parasite interactions, and abiotic changes beyond temperature.