Bioenergetic theory predicts infection dynamics of human schistosomes in intermediate host snails across ecological gradients

Abstract

Epidemiological dynamics depend on the traits of hosts and parasites, but hosts and parasites are heterogeneous entities that exist in dynamic environments. Resource availability is a particularly dynamic and potent environmental driver of within-host infection dynamics (temporal patterns of growth, reproduction, parasite production and survival). We developed, parameterised and validated a model for resource-explicit infection dynamics by incorporating a parasitism module into dynamic energy budget theory. The model mechanistically explained the dynamic multivariate responses of the human parasite Schistosoma mansoni and its intermediate host snail to variation in resources and host density. At the population level, feedbacks mediated by resource competition could create a unimodal relationship between snail density and human risk of exposure to schistosomes. Consequently, weak snail control could backfire if reductions in snail density release remaining hosts from resource competition. If resource competition is strong and relevant to schistosome production in nature, it could inform control strategies.

Elucidating mechanisms of invasion success: Effects of parasite removal on growth and survival rates of invasive and native frogs

“…Anthelmintic treatments increased 2‐week survival rates by 1.4% (Figure 1d; Table ), which compounds to a maximum of 2.4% after 2 months, and did not affect growth rates (Tables 1 and2; Figures 3 and 4). These small effects of parasitic worms on hosts were unexpected, given the potential costs of parasitic infections on hosts as host resources are consumed directly by parasites and additional energy is lost to immune defences and repair of tissues damaged by feeding, attachment and migration (Bonneaud et al., 2003; Civitello, Allman, Morozumi, & Rohr, 2018; Civitello, Fatima, Johnson, Nisbet, & Rohr, 2018; Cressler, Nelson, Day, & McCauley, 2014; Medzhitov, Schneider, & Soares, 2012). Frogs may have been able to compensate for energy lost to worms by increasing their food intake, as has been shown experimentally in captive Cuban treefrogs that were parasitized by A. hamatospicula (Knutie et al., 2017).…”

Deciphering the effect of food availability, growth and host condition on disease susceptibility in a marine invertebrate

“…Like their hosts, pathogenic organisms require energy resources to grow and reproduce. In food-restricted hosts, these resources may be reduced to levels that can limit pathogen growth (Civitello et al, 2018;Smith et al, 2005). For example, food-restricted zooplankton exposed to virulent fungal parasites died more slowly and exhibited fewer parasites than did wellfed ones (Hall et al, 2009).…”

Comparative analysis of time-based and quadrat sampling in seasonal population dynamics of intermediate hosts of human schistosomes

“…which typically occurred between October and March. Beyond the problem of compensatory feedbacks, the observation of density feedbacks warrants the evaluation of the effect of reductions in snail populations in terms of transmission potential to humans as subject to non-linearities in cercarial productivity with resource availability [35,36]. Novel approaches leveraging DNA-based tools such as PCR for the identification of snail and schistosome species [3], as well as environmental-DNA (eDNA) quantification techniques recently developed for schistosomes can play in important role in investigating these issues [64].…”

“…First and foremost density feedbacks determine the strength of populations rebounds that can be expected after treatment, also called compensatory density feedbacks as highlighted for O. hupensis in different types of habitats in China [34]. In addition, the reduction of snail abundance in the presence of negative density feedback could lead in certain cases to a net increase in cercarial production by the remaining infected snails due to the resulting per capita increase in limited resources [35]. This nonlinear link between snail density and cercariogenesis could thus potentially undermine the aim of reducing transmission through snail control [36].…”