Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts

Neal T Halstead,Christopher M Hoover,Steve A Johnson,Nicolas Jouanard,Karena Nguyen,Arathi Arakala,Taegan A Mcmahon,Gilles Riveau,Kristin A Loerns,David J Civitello,Susanne H Sokolow,Raphael A Ndione,Giulio A De Leo,Thomas R Raffel,Jason R Rohr,Justin V Remais,Manoj Gambhir

doi:10.1038/s41467-018-03189-w

Abstract

Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries. Increased prevalence and spread of human schistosomiasis to non-endemic areas has been consistently linked with water resource management related to agricultural expansion. However, the role of agrochemical pollution in human schistosome transmission remains unexplored, despite strong evidence of agrochemicals increasing snail-borne diseases of wildlife and a projected 2- to 5-fold increase in global agrochemical use by 2050. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, a herbicide, and an insecticide, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat and decreasing densities of snail predators. Epidemiological models indicate that these agrochemical effects can increase transmission of schistosomes. Identifying agricultural practices or agrochemicals that minimize disease risk will be critical to meeting growing food demands while improving human wellbeing.

Highlights

Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries
Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, a herbicide, and an insecticide, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat and decreasing densities of snail predators
We created outdoor freshwater pond communities consisting of two snail predators, three snail species (Biomphalaria glabrata [native to the Neotropics, introduced to Africa; an intermediate host of Schistosoma mansoni], Bulinus truncatus [native to Africa, the Middle East, and parts of southern Europe; an intermediate host of Schistosoma haematobium], and Haitia cubensis [a non-host snail species native to the Caribbean and southeastern United States]), zooplankton, and algae in 60 1200 L mesocosms filled with 800 L of water

Summary

Introduction

Schistosomiasis is a snail-borne parasitic disease that ranks among the most important water-based diseases of humans in developing countries. Using a field mesocosm experiment, we show that environmentally relevant concentrations of fertilizer, a herbicide, and an insecticide, individually and as mixtures, increase densities of schistosome-infected snails by increasing the algae snails eat and decreasing densities of snail predators. We use a field mesocosm experiment to demonstrate that environmentally relevant concentrations of agrochemicals (fertilizer, the herbicide atrazine, and the insecticide chlorpyrifos) increase the densities of schistosome-infected snails. These effects occur through both bottom-up effects by increasing the algae snails eat (fertilizer and atrazine) and top-down effects by decreasing densities of snail predators (chlorpyrifos). We developed epidemiological models that indicate that these agrochemical effects can increase transmission of schistosomes to humans

Methods

Results

Conclusion