Long-term prevalence data reveals spillover dynamics in a multi-host (Artemia), multi-parasite (Microsporidia) community

In the study of multi-host parasites, it is often found that host species contribute asymmetrically to parasite transmission, with cascading effects on parasite dynamics and overall community structure. Yet, identifying which of the host species contribute to parasite transmission and maintenance is a recurring challenge. Here, we approach this issue by taking advantage of natural variation in the community composition of host species. We studied the horizontally transmitted microsporidians Anostracospora rigaudi and Enterocytospora artemiae in a Southern French metacommunity of their brine shrimp hosts, Artemia franciscana and Artemia parthenogenetica. Within the metacommunity, patches can contain either or both of the Artemia host species, so that long-term prevalence data can provide a direct link between the presence of the two host species and the persistence of the two parasites. First, we show that the microsporidian A. rigaudi is a spillover parasite: it was unable to persist in the absence of its maintenance host A. parthenogenetica. This result was particularly striking in light of A. rigaudis high prevalence (in the field) and high infectivity (when tested in the lab) in both hosts. Moreover, A. parthenogeneticas seasonal presence imposed seasonality on the rate of spillover, causing cyclical pseudo-endemics in the spillover host A. franciscana. Second, while our prevalence data was sufficient to identify E. artemiae as either a spillover or a facultative multi-host parasite, we could not distinguish between the two possibilities. This study supports the importance of studying the community context of multi-host parasites, and demonstrates that in appropriate multi-host systems, sampling across a range of conditions and host communities can lead to clear conclusions about the drivers of parasite persistence.