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Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis

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 treatmen...

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Autores principales: Haggerty, Christopher J. E., Bakhoum, Sidy, Civitello, David J., De Leo, Giulio A., Jouanard, Nicolas, Ndione, Raphael A., Remais, Justin V., Riveau, Gilles, Senghor, Simon, Sokolow, Susanne H., Sow, Souleymane, Wolfe, Caitlin, Wood, Chelsea L., Jones, Isabel, Chamberlin, Andrew J., Rohr, Jason R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7365472/
https://www.ncbi.nlm.nih.gov/pubmed/32628666
http://dx.doi.org/10.1371/journal.pntd.0008417
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author Haggerty, Christopher J. E.
Bakhoum, Sidy
Civitello, David J.
De Leo, Giulio A.
Jouanard, Nicolas
Ndione, Raphael A.
Remais, Justin V.
Riveau, Gilles
Senghor, Simon
Sokolow, Susanne H.
Sow, Souleymane
Wolfe, Caitlin
Wood, Chelsea L.
Jones, Isabel
Chamberlin, Andrew J.
Rohr, Jason R.
author_facet Haggerty, Christopher J. E.
Bakhoum, Sidy
Civitello, David J.
De Leo, Giulio A.
Jouanard, Nicolas
Ndione, Raphael A.
Remais, Justin V.
Riveau, Gilles
Senghor, Simon
Sokolow, Susanne H.
Sow, Souleymane
Wolfe, Caitlin
Wood, Chelsea L.
Jones, Isabel
Chamberlin, Andrew J.
Rohr, Jason R.
author_sort Haggerty, Christopher J. E.
collection PubMed
description 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.
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spelling pubmed-73654722020-07-27 Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis Haggerty, Christopher J. E. Bakhoum, Sidy Civitello, David J. De Leo, Giulio A. Jouanard, Nicolas Ndione, Raphael A. Remais, Justin V. Riveau, Gilles Senghor, Simon Sokolow, Susanne H. Sow, Souleymane Wolfe, Caitlin Wood, Chelsea L. Jones, Isabel Chamberlin, Andrew J. Rohr, Jason R. PLoS Negl Trop Dis Research Article 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. Public Library of Science 2020-07-06 /pmc/articles/PMC7365472/ /pubmed/32628666 http://dx.doi.org/10.1371/journal.pntd.0008417 Text en © 2020 Haggerty et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Haggerty, Christopher J. E.
Bakhoum, Sidy
Civitello, David J.
De Leo, Giulio A.
Jouanard, Nicolas
Ndione, Raphael A.
Remais, Justin V.
Riveau, Gilles
Senghor, Simon
Sokolow, Susanne H.
Sow, Souleymane
Wolfe, Caitlin
Wood, Chelsea L.
Jones, Isabel
Chamberlin, Andrew J.
Rohr, Jason R.
Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis
title Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis
title_full Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis
title_fullStr Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis
title_full_unstemmed Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis
title_short Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis
title_sort aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7365472/
https://www.ncbi.nlm.nih.gov/pubmed/32628666
http://dx.doi.org/10.1371/journal.pntd.0008417
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