Variability in environmental persistence but not per capita transmission rates of the amphibian chytrid fungus leads to differences in host infection prevalence.

Heterogeneities in infections among host populations may arise through differences in environmental conditions through two mechanisms. First, environmental conditions may alter host exposure to pathogens via effects on survival. Second, environmental conditions may alter host susceptibility, making infection more or less likely if contact between a host and pathogen occurs. Further, host susceptibility might be altered through acquired resistance, which hosts can develop, in some systems, through exposure to dead or decaying pathogens and their metabolites. Environmental conditions may alter the rates of pathogen decomposition, influencing the likelihood of hosts developing acquired resistance. The present study primarily tests how environmental context influences the relative contributions of pathogen survival and per capita transmission on host infection prevalence using the amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) as a model system. Secondarily, we evaluate how environmental context influences the decomposition of Bd because previous studies have shown that dead Bd and its metabolites can illicit acquired resistance in hosts. We conducted Bd survival and infection experiments and then fit models to discern how Bd mortality, decomposition and per capita transmission rates vary among water sources [e.g. artificial spring water (ASW) or water from three ponds]. We found that infection prevalence differed among water sources, which was driven by differences in mortality rates of Bd, rather than differences in per capita transmission rates. Bd mortality rates varied among pond water treatments and were lower in ASW compared to pond water. These results suggest that variation in Bd infection dynamics could be a function of environmental factors in waterbodies that result in differences in exposure of hosts to live Bd. In contrast to the persistence of live Bd, we found that the rates of decomposition of dead Bd did not vary among water sources, which may suggest that exposure of hosts to dead Bd or its metabolites might not commonly vary among nearby sites. Ultimately, a mechanistic understanding of the environmental dependence of free-living pathogens could lead to a deeper understanding of the patterns of outbreak heterogeneity, which could inform surveillance and management strategies.

Batrachochytrium dendrobatidis in the Arid and Thermally Extreme Sonoran Desert.

Batrachochytrium dendrobatidis (Bd), the causative agent of the devastating global amphibian disease chytridiomycosis, was not projected to threaten amphibians in hot and arid regions due to its sensitivity to heat and desiccation. However, Bd is being detected more frequently than ever in hot and arid regions of Australia and the USA, challenging our current understanding of the environmental tolerances of the pathogen under natural conditions. We surveyed for Bd in an extremely hot and arid portion of the Sonoran Desert, where the pathogen is not projected to occur, and related presence and prevalence of the pathogen to local environmental conditions. We collected eDNA samples from isolated desert water sites including six tinajas and 13 catchments in June and August of 2020 and swabbed a total of 281 anurans of three species (red-spotted toad Anaxyrus punctatus, Couch's spadefoot Scaphiopus couchii, and the Sonoran Desert toad Incillius alvarius) across five catchments and six tinajas from June to September of 2020. Overall, Bd occurred at 68.4% of sites, despite extreme heat and aridity routinely exceeding tolerances established in laboratory studies. Average summer maximum air and water temperatures were 40.7°C and 30.7°C, respectively, and sites received an average of just 16.9 mm of precipitation throughout the summer monsoon season. Prevalence was low (5.7%) across species and life stage. Our results demonstrate that Bd is capable of persisting and infecting amphibians beyond its projected range, indicating a need to account for higher thermal tolerances when quantifying risk of Bd presence and infection.