Predicting disease dynamics and human infection risk from wildlife requires a strong understanding of the traits of hosts and parasites. However, hosts and parasites are not uniform entities that exist in constant environments. Instead, organisms can vary dramatically and the environment is heterogeneous across space and time. We developed a bioenergetics framework that integrates the intrinsic traits of hosts and parasites (e.g., body size and underlying physiology) with the influence of external factors (e.g., resource availability) to mechanistically predict infection dynamics for individual hosts. We parameterized and validated the model with microcosm experiments that manipulated host and resource density using the major human parasite Schistosoma mansoni and its intermediate snail host, Biomphalaria glabrata. The model predicts strong negative host density dependence on rates of parasite production per snail host, potentially severing the classically assumed link between infected intermediate host density and human risk of exposure. We then tested these predictions by manipulating the size structure and resource supply rates of experimental snail populations and creating experimental epidemics.
Results/Conclusions
The parameterized bioenergetics model of infection dynamics predicts that increases in snail host density could reduce parasite production rates by ~3 orders of magnitude relative to competition-free controls potentially driving a negative relationship between host density and ecological risk of human exposure. The experimental epidemics confirmed this prediction. As host densities rose in the experiment, parasite production rates per snail host declined from ~1000-3000 parasites per day to ~1-20. Variation in parasite production rates, rather than density of infected hosts, explained ~85% of the variation in human risk of exposure, measured as the total production rate of cercariae per mesocosm. A mixed model revealed that the total biomass of the snail population was the best predictor of individual parasite production rates, consistent with the predicted strong role of resource competition in limiting parasite production within infected hosts. These results illustrate a strong negative relationship between host density and human risk, driven by resource competition among intermediate hosts. Ultimately, current methods for estimating and reducing human risk may backfire if reductions in intermediate host density can release remaining hosts from resource competition.