Beyond temperature: Comparing the roles of temperature, nutrients and evaporation on parasite seasonality and amphibian disease risk in natural systems

Background/Question/Methods

There is a growing need to understand how multiple environmental stressors simultaneously influence disease risk; however, parasite transmission is a complex process, which is driven by host and parasite demographics as well as changes to their interactions.  The multifaceted nature of some stressors, such as climate change, introduces further complexity.  The goal of this study was to understand the relative influence of climate variables (growing degree days, diurnal temperature range, and evaporation rate) and nutrients on interactions between two trematode parasite species and their intermediate hosts (aquatic snails and larval amphibians).  Both species are transmitted from snail hosts to larval amphibians, and infection of early-stage tadpoles can lead to mortality or severe limb deformities. Between May and August 2010, we visited 20 wetlands in the East Bay region of California four times (80 total site visits).  We used dataloggers to continuously record temperatures and quantified snail density, the percentage of infected snails, tadpole developmental stages, and metamorph deformity rates at each visit.  We also counted the parasites in metamorphs collected during the June visit, and measured dissolved phosphorus and nitrogen in July.  We used an information theoretic approach to find models that best explained host density, infection and pathology.

Results/Conclusions

While temperature predicted increases in the percentage of infected snails at late-season visits, amphibian infections were best explained by a negative association with evaporation rate, and nutrients were the strongest positive predictor of amphibian deformities.  Amphibian deformities were best predicted by the density of infected snails in early summer (May and June), suggesting that seasonal changes in parasite abundance are important for host pathology.  Furthermore, the effect of temperature on the percentage of infected snails differed in early and late season.  The best models to explain snail infection prevalence included a time-by-temperature interaction, such that increases in infection prevalence with temperature only occurred at the later visits.  Thus, although temperature influenced parasite infection in snails, this effect occurred too late to have a large impact on tadpole infections.  Rather, negative associations between evaporation rates and the density of infected snails likely explained the lower infections found in metamorphic frogs at wetlands with high evaporation rates.  Despite the influence of evaporation on amphibian infection levels, nutrients were actually the strongest predictor of amphibian deformities.  Our study highlights the importance of considering a wide spectrum of environmental stressors and their net influence on host and parasite abundance and interactions.