Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.
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This content will become publicly available on September 13, 2024
Temperature affects predation of schistosome-competent snails by a novel invader, the marbled crayfish Procambarus virginalis
The human burden of environmentally transmitted infectious diseases can depend strongly on ecological factors, including the presence or absence of natural enemies. The marbled crayfish (
- Award ID(s):
- 2022321
- NSF-PAR ID:
- 10475812
- Editor(s):
- Mancinelli, Giorgio
- Publisher / Repository:
- PLoS One
- Date Published:
- Journal Name:
- PLOS ONE
- Volume:
- 18
- Issue:
- 9
- ISSN:
- 1932-6203
- Page Range / eLocation ID:
- e0290615
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Swimmer's itch is an emerging disease caused by flatworm parasites that often use water birds as definitive hosts. When parasite larvae penetrate human skin they initiate localized inflammation that leads to intense itching. Concerns about this issue have been growing recently due to an apparent increase in the global occurrence of swimmer's itch and its subsequent impacts on recreational activities and associated revenues. Past study has identified the common merganser as a key definitive host for these worms in the United States; a number of snail species serve as intermediate hosts. Although previous attempts at controlling swimmer's itch have targeted snails, a handful of efforts have concentrated on treating water birds with the anthelmintic drug, praziquantel. We construct a mathematical model of swimmer's itch and its treatment within the infected merganser population. Our goal is to identify merganser treatment regimes that minimize the number of infected snails thereby reducing the risk of human infections. Optimal control of bird hosts is defined analytically and we include numerical simulations assuming different resource‐allocation strategies. Results from the study may help identify treatment protocols that lower merganser infection rates and ultimately reduce the occurrence of swimmer's itch in freshwater systems throughout the Midwest.
Recommendations for Resource Managers Regardless of the time and monetary resources available, praziquantel treatment frequency should increase as mergansers arrive on the lake with continued treatments (albeit at reduced levels) until the end of the residency period.
Allocating plenty of resources towards the treatment of mergansers predicted a sharp drop in infected birds, which then remained close to zero throughout the remainder of the residency period. This approach reduced schistosome infection in mergansers and kept snail infections within the idealized range during times of peak recreational activity. Consequently, human cases of swimmer's itch would be expected to be low to nonexistent. Furthermore, our treatment‐longevity computation suggested that subsequent praziquantel dosing would not be required for a number of years.
Under more limited resources, the number of birds treated per day was much smaller throughout the residency period; however, even under these circumstances (which equated to treating approximately one bird every 5 days), simulated infected merganser densities were reduced to the point where snail infections remained below epidemic levels through to the end of the recreational period. Treatment longevity was shorter compared with the high‐resource option, but still extended 122 days into Season 2 (posttreatment).
We also used our model to investigate situations where lake managers and/or federal agencies might be taxed in terms of the time available to continuously treat mergansers on a given lake. An individual scientist may only have a single day (or two) to dose birds, rather than continuously administering praziquantel throughout the birds' residency period. If <77% of the total number of arriving birds can be treated in a single day, we recommend praziquantel administrations when the number of mergansers reaches the maximum that can be successfully treated. In addition, model simulations demonstrate that if managers are able to treat a large number of birds, they should wait until the end of the migration period.
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Abstract Predation on parasites is a common interaction with multiple, concurrent outcomes. Free‐living stages of parasites can comprise a large portion of some predators' diets and may be important resources for population growth. Predation can also reduce the density of infectious agents in an ecosystem, with resultant decreases in infection rates. While predator–parasite interactions likely vary with parasite transmission strategy, few studies have examined how variation in transmission mode influences contact rates with predators and the associated changes in consumption risk.
To understand how transmission mode mediates predator–parasite interactions, we examined associations between an oligochaete predator
Chaetogaster limnaei that lives commensally on freshwater snails and nine trematode taxa that infect snails.Chaetogaster is hypothesized to consume active (i.e. mobile), free‐living stages of trematodes that infect snails (miracidia), but not the passive infectious stages (eggs); it could thus differentially affect transmission and infection prevalence of parasites, including those with medical or veterinary importance. Alternatively, when infection does occur,Chaetogaster can consume and respond numerically to free‐living trematode stages released from infected snails (cercariae). These two processes lead to contrasting predictions about whetherChaetogaster and trematode infection of snails correlate negatively (‘protective predation’) or positively (‘predator augmentation’).Here, we tested how parasite transmission mode affected
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Chaetogaster limited the risk of snail infection and its subsequent pathology (i.e. castration). For taxa with passive infectious stages, no such protective effect was observed. Rather, infected snails were associated with higherChaetogaster abundance, likely owing to the resource subsidy provided by cercariae. These findings highlight the ecological and epidemiological importance of predation on free‐living stages while underscoring the influence of parasite life history in shaping such interactions. -
Secor, W. Evan (Ed.)Schistosome parasites infect more than 200 million people annually, mostly in sub-Saharan Africa, where people may be co-infected with more than one species of the parasite. Infection risk for any single species is determined, in part, by the distribution of its obligate intermediate host snail. As the World Health Organization reprioritizes snail control to reduce the global burden of schistosomiasis, there is renewed importance in knowing when and where to target those efforts, which could vary by schistosome species. This study estimates factors associated with schistosomiasis risk in 16 villages located in the Senegal River Basin, a region hyperendemic for Schistosoma haematobium and S . mansoni . We first analyzed the spatial distributions of the two schistosomes’ intermediate host snails ( Bulinus spp. and Biomphalaria pfeifferi , respectively) at village water access sites. Then, we separately evaluated the relationships between human S . haematobium and S . mansoni infections and (i) the area of remotely-sensed snail habitat across spatial extents ranging from 1 to 120 m from shorelines, and (ii) water access site size and shape characteristics. We compared the influence of snail habitat across spatial extents because, while snail sampling is traditionally done near shorelines, we hypothesized that snails further from shore also contribute to infection risk. We found that, controlling for demographic variables, human risk for S . haematobium infection was positively correlated with snail habitat when snail habitat was measured over a much greater radius from shore (45 m to 120 m) than usual. S . haematobium risk was also associated with large, open water access sites. However, S . mansoni infection risk was associated with small, sheltered water access sites, and was not positively correlated with snail habitat at any spatial sampling radius. Our findings highlight the need to consider different ecological and environmental factors driving the transmission of each schistosome species in co-endemic landscapes.more » « less
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