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Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis.
PLoS Negl Trop Dis. 2020 Jul; 14(7):e0008417.PN

Abstract

BACKGROUND

Schistosomiasis is responsible for the second highest burden of disease among neglected tropical diseases globally, with over 90 percent of cases occurring in African regions where drugs to treat the disease are only sporadically available. Additionally, human re-infection after treatment can be a problem where there are high numbers of infected snails in the environment. Recent experiments indicate that aquatic factors, including plants, nutrients, or predators, can influence snail abundance and parasite production within infected snails, both components of human risk. This study investigated how snail host abundance and release of cercariae (the free swimming stage infective to humans) varies at water access sites in an endemic region in Senegal, a setting where human schistosomiasis prevalence is among the highest globally.

METHODS/PRINCIPAL FINDINGS

We collected snail intermediate hosts at 15 random points stratified by three habitat types at 36 water access sites, and counted cercarial production by each snail after transfer to the laboratory on the same day. We found that aquatic vegetation was positively associated with per-capita cercarial release by snails, probably because macrophytes harbor periphyton resources that snails feed upon, and well-fed snails tend to produce more parasites. In contrast, the abundance of aquatic macroinvertebrate snail predators was negatively associated with per-capita cercarial release by snails, probably because of several potential sublethal effects on snails or snail infection, despite a positive association between snail predators and total snail numbers at a site, possibly due to shared habitat usage or prey tracking by the predators. Thus, complex bottom-up and top-down ecological effects in this region plausibly influence the snail shedding rate and thus, total local density of schistosome cercariae.

CONCLUSIONS/SIGNIFICANCE

Our study suggests that aquatic macrophytes and snail predators can influence per-capita cercarial production and total abundance of snails. Thus, snail control efforts might benefit by targeting specific snail habitats where parasite production is greatest. In conclusion, a better understanding of top-down and bottom-up ecological factors that regulate densities of cercarial release by snails, rather than solely snail densities or snail infection prevalence, might facilitate improved schistosomiasis control.

Authors+Show Affiliations

Department of Biological Sciences, Environmental Change Initiative, Eck Institute of Global Health, University of Notre Dame, Notre Dame, Indiana, United States of America. Department of Integrative Biology, University of South Florida, Tampa, Florida, United States of America.Université Cheikh Anta Diop, Dakar, Senegal.Department of Biology, Emory University, Atlanta, Georgia, United States of America.Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America.Station d'Innovation Aquacole, Saint-Louis, Senegal. Centre de Recherche Biomédicale Espoir pour la Santé, Saint-Louis, Senegal.Centre de Recherche Biomédicale Espoir pour la Santé, Saint-Louis, Senegal.Division of Environmental Health Sciences, School of Public Health, University of California, Berkeley, California, United States of America.Centre de Recherche Biomédicale Espoir pour la Santé, Saint-Louis, Senegal. Institut Pasteur de Lille-CIIL, France.Centre de Recherche Biomédicale Espoir pour la Santé, Saint-Louis, Senegal.Woods Institute for the Environment, Stanford University, Stanford, California, United States of America.Centre de Recherche Biomédicale Espoir pour la Santé, Saint-Louis, Senegal.College of Public Health, University of South Florida, Tampa, Florida, United States of America.School of Aquatic and Fishery Sciences, University of Washington, Seattle, Washington, United States of America.Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America.Department of Biology, Hopkins Marine Station, Stanford University, Pacific Grove, California, United States of America.Department of Biological Sciences, Environmental Change Initiative, Eck Institute of Global Health, University of Notre Dame, Notre Dame, Indiana, United States of America. Department of Integrative Biology, University of South Florida, Tampa, Florida, United States of America.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

32628666

Citation

Haggerty, Christopher J E., et al. "Aquatic Macrophytes and Macroinvertebrate Predators Affect Densities of Snail Hosts and Local Production of Schistosome Cercariae That Cause Human Schistosomiasis." PLoS Neglected Tropical Diseases, vol. 14, no. 7, 2020, pp. e0008417.
Haggerty CJE, Bakhoum S, Civitello DJ, et al. Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis. PLoS Negl Trop Dis. 2020;14(7):e0008417.
Haggerty, C. J. E., Bakhoum, S., Civitello, D. J., De Leo, G. A., Jouanard, N., Ndione, R. A., Remais, J. V., Riveau, G., Senghor, S., Sokolow, S. H., Sow, S., Wolfe, C., Wood, C. L., Jones, I., Chamberlin, A. J., & Rohr, J. R. (2020). Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis. PLoS Neglected Tropical Diseases, 14(7), e0008417. https://doi.org/10.1371/journal.pntd.0008417
Haggerty CJE, et al. Aquatic Macrophytes and Macroinvertebrate Predators Affect Densities of Snail Hosts and Local Production of Schistosome Cercariae That Cause Human Schistosomiasis. PLoS Negl Trop Dis. 2020;14(7):e0008417. PubMed PMID: 32628666.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis. AU - Haggerty,Christopher J E, AU - Bakhoum,Sidy, AU - Civitello,David J, AU - De Leo,Giulio A, AU - Jouanard,Nicolas, AU - Ndione,Raphael A, AU - Remais,Justin V, AU - Riveau,Gilles, AU - Senghor,Simon, AU - Sokolow,Susanne H, AU - Sow,Souleymane, AU - Wolfe,Caitlin, AU - Wood,Chelsea L, AU - Jones,Isabel, AU - Chamberlin,Andrew J, AU - Rohr,Jason R, Y1 - 2020/07/06/ PY - 2019/06/04/received PY - 2020/05/22/accepted PY - 2020/07/16/revised PY - 2020/7/7/pubmed PY - 2020/7/7/medline PY - 2020/7/7/entrez SP - e0008417 EP - e0008417 JF - PLoS neglected tropical diseases JO - PLoS Negl Trop Dis VL - 14 IS - 7 N2 - BACKGROUND: Schistosomiasis is responsible for the second highest burden of disease among neglected tropical diseases globally, with over 90 percent of cases occurring in African regions where drugs to treat the disease are only sporadically available. Additionally, human re-infection after treatment can be a problem where there are high numbers of infected snails in the environment. Recent experiments indicate that aquatic factors, including plants, nutrients, or predators, can influence snail abundance and parasite production within infected snails, both components of human risk. This study investigated how snail host abundance and release of cercariae (the free swimming stage infective to humans) varies at water access sites in an endemic region in Senegal, a setting where human schistosomiasis prevalence is among the highest globally. METHODS/PRINCIPAL FINDINGS: We collected snail intermediate hosts at 15 random points stratified by three habitat types at 36 water access sites, and counted cercarial production by each snail after transfer to the laboratory on the same day. We found that aquatic vegetation was positively associated with per-capita cercarial release by snails, probably because macrophytes harbor periphyton resources that snails feed upon, and well-fed snails tend to produce more parasites. In contrast, the abundance of aquatic macroinvertebrate snail predators was negatively associated with per-capita cercarial release by snails, probably because of several potential sublethal effects on snails or snail infection, despite a positive association between snail predators and total snail numbers at a site, possibly due to shared habitat usage or prey tracking by the predators. Thus, complex bottom-up and top-down ecological effects in this region plausibly influence the snail shedding rate and thus, total local density of schistosome cercariae. CONCLUSIONS/SIGNIFICANCE: Our study suggests that aquatic macrophytes and snail predators can influence per-capita cercarial production and total abundance of snails. Thus, snail control efforts might benefit by targeting specific snail habitats where parasite production is greatest. In conclusion, a better understanding of top-down and bottom-up ecological factors that regulate densities of cercarial release by snails, rather than solely snail densities or snail infection prevalence, might facilitate improved schistosomiasis control. SN - 1935-2735 UR - https://www.unboundmedicine.com/medline/citation/32628666/Aquatic_macrophytes_and_macroinvertebrate_predators_affect_densities_of_snail_hosts_and_local_production_of_schistosome_cercariae_that_cause_human_schistosomiasis L2 - https://dx.plos.org/10.1371/journal.pntd.0008417 DB - PRIME DP - Unbound Medicine ER -
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