Hot bodies protect amphibians against chytrid infection in nature

Abstract

Environmental context strongly affects many host-pathogen interactions, but the underlying causes of these effects at the individual level are usually poorly understood. The amphibian chytrid fungus has caused amphibian population declines and extinctions in many parts of the world. Many amphibian species that have declined or have been extirpated by the pathogen in some environments coexist with it in others. Here we show that in three species of rainforest frogs in nature, individuals' probability of infection by the amphibian chytrid fungus was strongly related to their thermal history. Individuals' probability of infection declined rapidly as they spent more time above the pathogen's upper optimum temperature. This relationship can explain population-level patterns of prevalence in nature, and suggests that natural or artificial selection for higher thermal preferences could reduce susceptibility to this pathogen. Similar individual-level insights could improve our understanding of environmental context-dependence in other diseases.

Figure 1. Individual probability of infection by the amphibian chytrid skin fungus and individual thermal history in nature.

(a) Prevalence of Bd infection in tracked frogs by species and gender and by season. Bars represent binomial (Clopper-Pearson) 95% confidence limits. (b) Boxplots illustrating distribution of percent of frog body temperatures above 25°C by species and gender and by season. Heavy bars represent medians, boxes represent 25% and 75% quartile boundaries, whiskers represent ranges, and stars are points outside 1.5× the interquartile range from the nearest quartile boundary. Comparing (a) and (b) suggests an inverse relationship between prevalence and percent of body temperatures above 25°C; this relationship was explored statistically in the models presented in Table 2.

Figure 2. Individual probability of infection by the amphibian chytrid skin fungus in nature was strongly related to individual thermal history.

This logistic model, incorporating species identity, gender, and percent of body temperatures above 25°C (Table 2), was produced by averaging the three best fitted models, each with delta AICC < 3. Color coding corresponds to species-level susceptibility to epidemic chytridiomycosis (red most, amber intermediate, green least). Predictions of the model correspond well (r² = 0.739, 4 d.f., P = 0.028) with population-level patterns of prevalence when it is used to predict prevalence by season and site, factors not included in the model.