Disease dynamics depend sensitively on the transmission of parasites among hosts. The mechanistic underpinnings of transmission determine the ability of parasites to initiate epidemics, the persistence of host populations once epidemics start, and the efficacy of disease management. Mechanistic, yet general representations of transmission can link individual behavior with disease spread, catalyzing novel insights into the ecological constraints and evolutionary implications of disease. Here we develop and test mechanistic models for transmission using a case study of fungal disease in a freshwater zooplankton. In this system, as in many others, hosts become infected after consuming free-living parasites. Starting with a classic density-dependent transmission model, we built several alternative models using components of foraging ecology of hosts: the consumption of parasites and interference competition among foraging hosts. Each model made distinct predictions for transmission rate given varying densities of host and parasite. Therefore, we used model selection to compare their predictions to experimental data. Then, we embedded these transmission submodels into a general, fully dynamic epidemiological model to determine their consequences for population-level metrics of epidemics. Finally, we tested an unexpected prediction from the best-performing model by assessing the relationship between initial host density and epidemic size in natural Daphnia populations.
Results/Conclusions
In the infection experiment, prevalence increased with parasite density, but decreased with host density. Additionally, foraging hosts consumed (and removed) most parasites from their habitat, but their per capita foraging rate decreased with increasing host density (through interference). Accordingly, the transmission model with consumption of parasites by hosts with density-dependent foraging rates outcompeted all others in the model selection. Once embedded into an epidemiological model, this transmission mechanism revealed an unexpected result: the parasite’s basic reproductive ratio (R0) and equilibrial prevalence of infection became unimodal functions of host density without disease. These predictions contradict the monotonically increasing density-R0 and density-prevalence relationships anticipated by the classic model. In our new model, low host densities inhibited disease spread (as in the classic case), but low rate of host-parasite contact (foraging) also inhibited disease spread at high host densities. Field data supported this prediction. In a survey of 19 lakes, we uncovered a unimodal relationship between initial host density and epidemic size. More generally, our results highlight how mechanistic links between host behavior and transmission can reveal broad, new insights into a variety of disease systems in which hosts consume parasites.