Disease as a moving target: Factors influencing infection ‘hotspots’ of a multi-host parasite across space and time

Background/Question/Methods

Heterogeneity is a hallmark of parasite and pathogen distributions, with both biotic and abiotic factors driving patchiness across a landscape.  Because host-parasite-environment interactions occur over different spatial and temporal scales, the factors associated with high parasite prevalence are also likely to be scale-dependent, highlighting the importance of cross-scale analyses of variation in disease risk.  We studied the dynamics of the trematode parasite, Ribeiroia ondatrae, which castrates snail hosts and frequently causes limb deformities in amphibian hosts.  To determine whether R. ondatrae hotspots shift in space and time, we re-surveyed 49 wetlands in 2010 distributed across the western US (California, Oregon, Washington, Montana) that had previously been sampled in 1999, and also monitored 17 northern California ponds at both a yearly (2009 and 2010) and a seasonal (four visits/season) interval.  To determine whether certain environmental or community factors were associated with these hotspots, we also recorded invertebrate and amphibian density and diversity, wetland depth, size, hydroperiod, temperature, and nutrient concentrations at each pond.

Results/Conclusions

We found that while the presence of R. ondatrae at a wetland was relatively stable through time, a wetland’s status as a ‘hotspot’ for R. ondatrae infection varied over a decade, across years, and within a single season.  In ponds measured a decade apart, 25% of wetlands gained R. ondatrae while 27% lost the parasite, usually due to loss of the necessary snail intermediate hosts, suggesting that snails are a primary limiting factor for infection.  At the annual scale, 42% of wetlands gained hotspot status from 2009 to 2010, while 60% exhibited reductions to below hotspot infection levels.  While snail host densities had no effect on annual variation in hotspots, we found spatial clustering, suggesting that factors varying regionally (i.e. prevalence in birds, or environmental characteristics) are likely important for annual changes in disease risk.  High within-season variation in prevalence of snails with mature infections was not due to steady increases in prevalence over the season as expected.  Instead, whether a pond was a hotspot in early or late season was a function of snail biomass which fluctuated nonlinearly.  Factors associated with variation in disease risk differ across scales, and better understanding of this phenomenon will improve wildlife disease management.