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

Abstract

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.

Infection burdens and virulence under heat stress: ecological and evolutionary considerations

“…The resources available to a parasite are directly linked to the pool of resources available to its host. How much host resource is given to the parasite can vary, depending on a range of factors, including the stage of infection, population density, host sex and manipulation of host physiology [97][98][99][100][101][102]. A host could increase its resource intake to accommodate the additional stress of infection (e.g.…”

Host-pathogen interactions under pressure: a systematic review and meta-analysis of stress-mediated effects on disease dynamics

“…A third explanation could be that hosts under limited resources could be smaller, and small hosts may carry fewer pathogens, therefore decreasing pathogen intensity within host. This has been reported in the snail-Schistosome system, where smaller snails carry fewer parasites (Civitello et al 2022). Moreover, in Daphnia populations, food shortage reduced body size with subsequent reductions in spore loads of a microsporidian parasite (Pulkkinen & Ebert 2004).…”

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

“…Water hyacinth invasion suppressed snail abundance more than total snail biomass; indicating that snails in this treatment were larger, on average, than in other treatments. Given that larger size and greater per capita access to food resources increase production of cercariae by infected snails (Civitello et al, 2018(Civitello et al, , 2022, these simultaneous effects could explain the increase in cercariae production. Water hyacinth invasion also appeared to suppress snail reproduction (Figure 2d).…”

“…Human schistosomes currently infect ~200 million people and cause schistosomiasis, a neglected tropical disease that contributes substantially to human morbidity (World Health Organization, 2021). Humans become infected by cercariae, a free‐swimming schistosome life stage released by infected snails, and total cercarial production, a determinant of transmission potential, increases with the abundance of infected snails and the quantity and quality of food resources available to each snail (Civitello et al, 2022; Steinmann et al, 2006). Some of the world's most intense hotspots of schistosome transmission, such as Lake Victoria, are also heavily invaded by nonnative aquatic macrophytes (Mutuku et al, 2019; Wanyonyi, 2019).…”