Size‐asymmetric competition among snails disrupts production of human‐infectious Schistosoma mansoni cercariae

Abstract

Parasites can harm hosts and influence populations, communities, and ecosystems. However, parasites are reciprocally affected by population‐ and community‐level dynamics. Understanding feedbacks between infection dynamics and larger‐scale epidemiological and ecological processes could improve predictions and reveal novel control methods. We evaluated how exploitative resource competition among hosts, a fundamental aspect of population biology, influences within‐host infection dynamics of the widespread human parasite Schistosoma mansoni in its intermediate host, Biomphalaria glabrata. We added size‐dependent consumption of shared resources to a parameterized bioenergetics model to predict a priori the growth, parasite production, and survival of an infected focal host coexisting with an uninfected conspecific competitor in an experiment that varied competitor size. The model quantitatively anticipated that competitors disrupt growth and parasite production and that these effects increase with competitor size. Fitting the model to these data improved its match to host survivorship. Thus, resource competition alters infection dynamics, there are strong size asymmetries in these effects, and size‐asymmetric resource competition effects on infection dynamics can be accurately predicted by bioenergetics theory. More broadly, this framework can assess parasite transmission and control in other contexts, such as in resource competitive host communities, or in response to eutrophication, food supplementation, or culling.

Multi-strain compatibility polymorphism between a parasite and its snail host, a neglected vector of schistosomiasis in Africa

“…Energy diverted from reproduction after parasitic castration is converted to enhanced snail growth and thus parasite growth ( Baudoin, 1975 ; Sorensen & Minchella, 2001 ; Lafferty & Kuris, 2009 ; Faro et al., 2013 ). Additionally, high quality nutrient diets, or increased availability of nutrients, such as through reduced competition, results in larger snails that produce more cercariae ( Sandland & Minchella, 2003 ; Civitello et al., 2020 ; Civitello & Hartman, 2021 ; Desautels et al., 2022 ), which in turn increases transmission likelihood of schistosomes to definitive host populations.…”

Experimental water hyacinth invasion and destructive management increase human schistosome transmission potential

“…Both snails and schistosomes respond positively to resource availability, increasing the number of snails and per‐snail productivity of human‐infectious cercariae with high resource quality or quantity (Civitello et al, 2018). However, as snails grow, they also reproduce, which intensifies competition for resources and limits cercariae production (Civitello et al, 2018; Civitello & Hartman, 2021; Malishev & Civitello, 2019). While destruction of water hyacinth increased reproduction (Figure 3d), new individuals in smaller size classes were almost never observed in the populations during weekly censusing while the number of large adult individuals remained relatively constant, i.e., there were consistent recruitment failures coinciding with high adult survival (Figure 3b; Appendix S1: Figure S3).…”

Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts

“…Successful infections add parasite biomass to an individual snail’s DEB model. Each susceptible and infected snail follows its own DEB model for resource consumption, growth, reproduction, survival, and production of parasite cercariae ( 29 , 38 , 51 ), which is integrated over the duration of the timestep. Algal resources grow logistically and are consumed by all snails in the population.…”