Spillover dynamics and asynchronous temporal fluctuations in host density and competence drive fungal parasite persistence in multi-host, seasonal communities.

Parasites routinely persist in seasonal systems while infecting multiple host species. An important question for parasite control is whether parasite persistence is driven by particular host species, specific times of year or their interaction. We have few empirically tractable models to answer this question. We develop a data-driven model that partitions species-specific and temporal drivers of parasite persistence from commonly collected surveillance data. Leveraging standard epidemiological theory, our approach demonstrates a novel way to link time-varying fluctuations in species-level contributions to parasite persistence directly to time-integrated parasite persistence in the community as a whole, while using real-world field data that is tractable to obtain. We applied our approach to 3 years of parasite surveillance data in seasonal amphibian communities persisting with the fungal pathogen Batrachochytrium dendrobatidis (Bd). We asked three questions: (i) Do amphibians trade-off in their contributions to Bd persistence across the year? (ii) What host characteristics, such as seasonally fluctuating host density or host competence, drive these trade-offs? and (iii) what are the relative contributions of species compared to periods of high transmission for enzootic Bd persistence? We found that the identity of the amphibian species driving Bd persistence was highly variable through time. Specifically, temporal variability in host density and less so variability in host competence drove the temporal variation in species' contributions to persistence. Moreover, our model identified two distinct mechanisms of Bd persistence: (i) spillover dynamics from a dominant maintenance species and (ii) temporally asynchronous, but equal, contributions of host species to persistence. In both cases, species-targeted interventions were as effective or more effective than temporal control for reducing the capacity of Bd to persist. Broadly, our results demonstrate that species contributions to parasite persistence can have strong, asynchronous temporal variability, potentially limiting the effectiveness of targeted seasonal parasite control. Our model is designed to link closely with standard parasite surveillance data and is broadly applicable to other host-parasite systems where it can partition who, when and what drive parasite persistence in multi-host seasonal communities.