LAUSR

Significance Predicting how ecological interactions among vectors or intermediate hosts of human parasites influence transmission potential to humans remains challenging. Here, we focus on human schistosomiasis and demonstrate how resource competition among snails profoundly alters the link between infected snails, the target of control, and schistosome cercariae, the cause of human infections. We integrated an individual-based bioenergetics model of snail and schistosome dynamics with experiments in artificial waterbodies and field observations to anticipate and explain how resource-sensitive schistosome infections and resource competition among snails interact to generate brief peaks in transmission potential when snail populations grow from low densities. A resource-explicit view of snail and schistosome dynamics could maximize the potential for snail control methods to contribute to control of schistosomiasis. Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.