Intraguild predation among snails drives human schistosome amplification despite susceptible host regulation

Competitors and predators of hosts can alter transmission dynamics within host-parasite systems. Biocontrol aims to harness these effects to mitigate disease, but these attempts may backfire without an understanding of the ecological interactions involved. We investigated how resource competition among snail species affects transmission potential of the human flatworm parasite Schistosoma mansoni from its snail intermediate host, Biomphalaria glabrata. We created experimental communities with B. glabrata, S. mansoni and differing compositions of non-host competitor snails Melanoides tuberculata and Physella acuta. We tracked resource availability, host abundance, size, reproduction and parasite production of cercariae, the schistosome life stage infectious to humans, over 16 weeks. We found that Melanoides acted as a typical resource competitor of Biomphalaria, reducing host body size and per capita cercarial production. Physella, however, reduced host abundance but increased resource availability and cercarial production. In follow-up experiments, we determined that Physella is a voracious consumer of host eggs. We then built a model representing this intraguild predation effect, which was able to explain these initially counterintuitive results. These divergent results from two putative resource competitors of Biomphalaria underscore the importance of establishing the mechanisms through which hosts, non-hosts and parasites interact, especially in the context of biocontrol.