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.

Keywords: asymmetric competition; energy budget; parasite production; parasitism; reproduction; resource competition.

Figure 1:

A priori predictions (lines), empirical results (points = means ± SE), and classic statistical test summaries from the size-dependent competition life table experiment for infected host traits as a function of uninfected competitor size. As predicted, (A) daily cercarial production and (B) final length of focal infected hosts significantly decreased with competitor size. However, (C) the a priori prediction that host survival would be unaffected by competitor size was not supported. Statistics in (A) and (B) are based on linear regression, whereas those in (C) are based on accelerated failure time survival analysis.

Figure 2:

A priori predictions of the bioenergetic model of infection applied to the size-asymmetric competition experiment. Temporal dynamics of growth, survival, and parasite production dynamics in an experiment manipulating infection in a focal host (columns) and the presence and initial size of an uninfected conspecific competitor (colors). Points represent treatment means ± SE. Prediction lines and shaded envelopes represent the median and 99% posterior credible interval of the mean dynamics of the bioenergetics model fit to these data. Growth of (A) infected and (B) uninfected focal hosts was substantially reduced by larger competitors. (C and D) These competitors grew substantially over the course of the experiment. (E) Infected hosts died slightly faster in the presence of larger competitors, but (F) uninfected hosts generally survived well. (G) Larger competitors reduced parasite production by focal hosts up to 14-fold. The model predicted these dynamics extremely well, with r_C ≥ 0.88 and AUC = 0.66 – 0.88. Notably, however, the model slightly overpredicted survival underpredicted early cercarial production for infected hosts across all treatments. Treatment means and SEs are calculated conditionally on host survival to each time point, so host mortality can (rarely) cause cumulative totals to decrease (e.g., for >15 mm competitor treatment in panel G).

Figure 3:

Updated predictions of the of the bioenergetic model of infection following direct parameterization to the outcome of the size-asymmetric competition experiment. Temporal dynamics of growth, survival, and parasite production dynamics in an experiment manipulating infection in a focal host (columns) and the presence and initial size of an uninfected conspecific competitor (colors). Points represent treatment means ± SE. Prediction lines and shaded envelopes represent the median and 99% posterior credible interval of the mean dynamics of the bioenergetics model fit to these data. Growth of (A) infected and (B) uninfected focal hosts was substantially reduced by larger competitors. (C and D) These competitors grew substantially over the course of the experiment. (E) Infected hosts died slightly faster in the presence of larger competitors, but (F) uninfected hosts generally survived well. (G) Larger competitors reduced parasite production by focal hosts up to 14-fold. The bioenergetics model explained these dynamics extremely well, with r_C > 0.90 and AUC = 0.64 – 0.89. Treatment means and SEs are calculated conditionally on host survival to each time point, so host mortality can (rarely) cause cumulative totals to decrease (e.g., for >15 mm competitor treatment in panel G).