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Nutritional effects of invasive macrophyte detritus on Schistosoma mansoni infections in snail intermediate hosts

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Abstract

Schistosomes are parasitic flatworms that cycle between humans and freshwater snails, infecting more than 200 million humans. Many schistosome-endemic sites are invaded by non-native plants that snails cannot consume. Inedible plants could suppress snail growth, reproduction, and schistosome production by outcompeting edible resources. Alternatively, their decomposition could create edible detritus that fuels snail growth, reproduction, or schistosome production. We evaluated the nutritional effects of detritus from four widespread invasive plants on human schistosomes, Schistosoma mansoni, and snail intermediate hosts, Biomphalaria glabrata. We predicted that water hyacinth, which is fibrous and waxy, would cause poor growth, reproduction, and parasite production. In contrast, we predicted water lettuce, water fern, and duckweed would enable rapid growth, reproduction, and parasite production via better nutrient content and digestibility. Infected snails consuming water fern and water lettuce grew ~ 100% larger and produced ~ ninefold more cercariae than those consuming water hyacinth or duckweed. We then tested whether extended decomposition of water hyacinth could improve snail and schistosome performance but found negligible effects. Managers should prioritize removal of plants that produce nutritious detritus, because in situ destruction could increase schistosome transmission. Characterizing interactions among plant invasions, management, and parasites could facilitate solutions that improve human and environmental health.

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Data availability

The datasets and analysis code generated during the current study are publicly available at a GitHub repository: https://github.com/DaveCivitello/Detritus_LTs. This repository will be made permanently available through Zenodo upon acceptance for publication. At that time, this statement will be amended to include a permanent DOI for the data and code.

Code availability

All data and code necessary to conduct analyses and produce figures is freely available: https://github.com/DaveCivitello/Detritus_LTs

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Acknowledgements

We thank the Civitello lab for feedback. The following reagents were obtained through BEI Resources, NIAID NIH: Schistosoma mansoni, Strain NMRI, Exposed Swiss Webster Mice, NR-21963, Biomphalaria glabrata Strain NMRI (Unexposed to Schistosoma mansoni), NR-21970. DJC was supported by the United States National Institute of Allergy and Infectious Diseases R01 AI150774.

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Authors and Affiliations

  1. Department of Biology, Emory University, 1510 Clifton Rd NE, Atlanta, GA, 30322, USA

    Daniel J. Desautels, Yebin Wang, Asher Ripp, Amber Beaman, Sena Andea, Rachel B. Hartman & David J. Civitello

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  1. Daniel J. Desautels
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  2. Yebin Wang
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  7. David J. Civitello
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Contributions

DJD and DJC conceived the experiments. DJD, YW, AR, AB, SA, and RBH conducted the experiments. DJD and DJC conducted the analysis. DJD wrote the first draft. All authors edited and approved the manuscript.

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Correspondence to David J. Civitello.

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Competing interest

DJC was supported by the United States National Institute of Allergy and Infectious Diseases R01 AI150774. The authors declare no competing interests.

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Desautels, D.J., Wang, Y., Ripp, A. et al. Nutritional effects of invasive macrophyte detritus on Schistosoma mansoni infections in snail intermediate hosts. Hydrobiologia 849, 3607–3616 (2022). https://doi.org/10.1007/s10750-022-04974-x

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