Thermal mismatch explains fungal disease dynamics in Brazilian frogs

Abstract

Theory predicts that susceptibility to disease in ectothermic hosts increases as temperatures depart from host’s thermal optima, because pathogens have functionally broader thermal tolerance ranges and acclimate faster than hosts to shifts in temperature. Hence, hosts adapted to cooler and warmer climates should be at greater risk of infection under abnormally warm and cool conditions, respectively. Batrachochytrium dendrobatidis (Bd) is a chytrid fungus that affects amphibians worldwide. In Brazil's Atlantic Forest, Bd outbreaks have been linked to numerous declines in amphibian populations, particularly in cooler high elevation areas. Thus, we hypothesize that years with abnormally warm temperatures could shift the balance in favor of the pathogen, thereby driving the historical declines. We also hypothesize that warm-adapted amphibians from lowland sites could experience elevated Bd infection risk during abnormally cold years. To test whether thermal mismatch (elevation vs. temperature anomaly) drove shifts in Bd prevalence through time we compiled a comprehensive database spanning 50 years, gathered across an elevational gradient within the Atlantic Forest. In agreement with our predictions, cool-adapted hosts had higher Bd prevalence when temperatures were higher than historical averages. In parallel, Bd prevalence in warm-adapted hosts was higher in colder-than-average years, although frogs from higher elevations exhibited an overall higher risk of disease due to disproportionally high infection prevalence. Our study links the thermal mismatch hypothesis with historical shifts in Bd prevalence in Brazilian frogs, indicating that Bd infections, modulated by climate change, may continue to have a negative impact on Neotropical amphibians.