Abstract
Human disease agents exist within complex environments that have underappreciated effects on transmission, especially for parasites with multi-host life cycles. We examined the impact of multiple host and parasite species on transmission of the human parasite Schistosoma mansoni in Kenya. We show S. mansoni is impacted by cattle and wild vertebrates because of their role in supporting trematode parasites, the larvae of which have antagonistic interactions with S. mansoni in their shared Biomphalaria vector snails. We discovered the abundant cattle trematode, Calicophoron sukari, fails to develop in Biomphalaria pfeifferi unless S. mansoni larvae are present in the same snail. Further development of S. mansoni is subsequently prevented by C. sukari's presence. Modeling indicated that removal of C. sukari would increase S. mansoni-infected snails by two-fold. Predictable exploitation of aquatic habitats by humans and their cattle enable C. sukari to exploit S. mansoni, thereby limiting transmission of this human pathogen.
Highlights
Infectious diseases exist in complex ecological settings and for some disease agents, successful transmission may require sequential colonization of multiple obligatory hosts
A portion of the field-collected Biomphalaria were exposed to S. mansoni to assess compatibility and we found that all three taxa of Biomphalaria were susceptible to S. mansoni, but found that B. pfeifferi was the most compatible (Figure 1d)
Both species were commonly recovered from B. pfeifferi, but C. sukari was not recovered from B. sudanica or B. choanomphala
Summary
Infectious diseases exist in complex ecological settings and for some disease agents, successful transmission may require sequential colonization of multiple obligatory hosts. As shown by an increasing number of studies, the net effect of biotically complex environments on transmission success for a particular parasite may be hard to predict, for parasites that use multiple hosts to complete their life cycles (Lafferty et al, 1994; Suzan et al, 2009; Lafferty, 2012; Johnson et al, 2013; Salkeld et al, 2013; Rohr et al, 2015; Frainer et al, 2018). The impact may be highly contextual, depending on the density of host species, leading to dilution or amplification of transmission (Luis et al, 2018). Another factor influencing the success of a particular parasite is the diversity of other infectious agents present that colonize the same host species, thereby setting up the potential for within-host interactions. The purpose of this study is to combine field observations, experimental infections and use of a mathematical model parameterized by our empirical data
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