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Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts

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. Hum...

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Autores principales: Civitello, David J., Angelo, Teckla, Nguyen, Karena H., Hartman, Rachel B., Starkloff, Naima C., Mahalila, Moses P., Charles, Jenitha, Manrique, Andres, Delius, Bryan K., Bradley, L. M., Nisbet, Roger M., Kinung’hi, Safari, Rohr, Jason R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8833218/
https://www.ncbi.nlm.nih.gov/pubmed/35121663
http://dx.doi.org/10.1073/pnas.2116512119
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author Civitello, David J.
Angelo, Teckla
Nguyen, Karena H.
Hartman, Rachel B.
Starkloff, Naima C.
Mahalila, Moses P.
Charles, Jenitha
Manrique, Andres
Delius, Bryan K.
Bradley, L. M.
Nisbet, Roger M.
Kinung’hi, Safari
Rohr, Jason R.
author_facet Civitello, David J.
Angelo, Teckla
Nguyen, Karena H.
Hartman, Rachel B.
Starkloff, Naima C.
Mahalila, Moses P.
Charles, Jenitha
Manrique, Andres
Delius, Bryan K.
Bradley, L. M.
Nisbet, Roger M.
Kinung’hi, Safari
Rohr, Jason R.
author_sort Civitello, David J.
collection PubMed
description 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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spelling pubmed-88332182022-08-04 Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts Civitello, David J. Angelo, Teckla Nguyen, Karena H. Hartman, Rachel B. Starkloff, Naima C. Mahalila, Moses P. Charles, Jenitha Manrique, Andres Delius, Bryan K. Bradley, L. M. Nisbet, Roger M. Kinung’hi, Safari Rohr, Jason R. Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2022-02-04 2022-02-08 /pmc/articles/PMC8833218/ /pubmed/35121663 http://dx.doi.org/10.1073/pnas.2116512119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Civitello, David J.
Angelo, Teckla
Nguyen, Karena H.
Hartman, Rachel B.
Starkloff, Naima C.
Mahalila, Moses P.
Charles, Jenitha
Manrique, Andres
Delius, Bryan K.
Bradley, L. M.
Nisbet, Roger M.
Kinung’hi, Safari
Rohr, Jason R.
Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts
title Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts
title_full Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts
title_fullStr Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts
title_full_unstemmed Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts
title_short Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts
title_sort transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8833218/
https://www.ncbi.nlm.nih.gov/pubmed/35121663
http://dx.doi.org/10.1073/pnas.2116512119
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