Resource fluctuations inhibit the reproduction and virulence of the human parasite Schistosoma mansoni in its snail intermediate host

Abstract

Resource availability can powerfully influence host–parasite interactions. However, we currently lack a mechanistic framework to predict how resource fluctuations alter individual infection dynamics. We address this gap with experiments manipulating resource supply and starvation for a human parasite, Schistosoma mansoni , and its snail intermediate host to test a hypothesis derived from mechanistic energy budget theory: resource fluctuations should reduce schistosome reproduction and virulence by inhibiting parasite ingestion of host biomass. Low resource supply caused hosts to remain small, reproduce less and produce fewer human-infectious cercariae. Periodic starvation also inhibited cercarial production and prevented infection-induced castration. The periodic starvation experiment also revealed substantial differences in fit between two bioenergetic model variants, which differ in their representation of host starvation. Simulations using the best-fit parameters of the winning model suggest that schistosome performance substantially declines with resource fluctuations with periods greater than 7 days. These experiments strengthen mechanistic theory, which can be readily scaled up to the population level to understand key feedbacks between resources, host population dynamics, parasitism and control interventions. Integrating resources with other environmental drivers of disease in an explicit bioenergetic framework could ultimately yield mechanistic predictions for many disease systems.

When should we expect predator biocontrol of human schistosomes to backfire?

“…Despite a dearth of laboratory studies evaluating the population dynamics of snails and schistosomes in response to a range of prawn densities, one laboratory study shows gape-limited predation by prawns can relax competition in populations of uninfected snails, yielding fewer, larger individuals that produce many eggs, consistent with predictions from the SIDEB model (Sokolow, Lafferty, and Kuris 2014). Although this experiment did not incorporate infection, recent experiments on resource competition and food supply suggest these conditions could promote high parasite yields from the remaining larger hosts (Civitello et al 2018(Civitello et al , 2020. Data on predator densities, feeding selectivity, dynamics of snail population densities and size-structure, cercariae shedding, and human infection are needed to critically evaluate these alternative hypotheses and thus effective predator biocontrol of human schistosomes.…”

“…The native African river prawn,Macrobrachium vollenhovenii, is a natural predator of snails and, recently, its local population collapse coincided with a large outbreak of human schistosomiasis in the Senegal River Basin (Sokolow, Lafferty, and Kuris 2014;Sokolow et al 2015).We identify and evaluate three key ecological mechanisms that drive 'do or do not' control responses in parasites and vectors. First, strong laboratory and field evidence shows snail populations compete over resources (Perez-Saez et al 2016;Preston and Sauer 2020;Civitello et al 2020). Second, production of human-infectious cercariae per snail increases steeply with resources (Civitello et al 2018), increasing host infectiousness with access to more food, as seen broadly for trematodes of humans and wildlife (Johnson et al 2007).…”

“…The infection rate of susceptible snail hosts is based on a constant daily introduction rate of free-living miracidia and host and parasite DEB parameters are from experiments on manipulated resource supply rates and periodic starvation periods (Civitello et al 2020). We simulated a 150-day season of host and parasite infection rates and densities resembling the typical schistosomiasis transmission season.…”

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

“…We used a bioenergetic model for infection dynamics that we previously derived and parameterized with experiments on individual snails (Civitello et al 2020) to make a priori predictions for the outcome of this competition experiment and then updated our parameterization by fitting the model to these results. Each snail is represented by the same model, which (if the snail is infected) incorporates a population of parasites that consume host resources, grow, reproduce, and cause damage into “standard” dynamic energy budget (DEB) theory for a free‐living host (Kooijman 2010).…”

“…Here we generate and test quantitative a priori predictions for the effects of size‐asymmetric competition among snails on infection dynamics of the major human parasite Schistosoma mansoni . Schistosome infections are much more productive and virulent when snail intermediate hosts have greater or more consistent access to food resources, which can be quantitatively explained using dynamic energy budget (DEB) theory models that treat parasites as a within‐snail population of consumers (Civitello et al 2018, 2020). Our parameterized DEB model predicts that uninfected snail competitors inhibit schistosome production and virulence in a focal infected host by limiting resource acquisition and that these inhibitory effects grow with competitor size.…”