Agricultural pesticides do not suppress infection of Biomphalaria (Gastropoda) by Schistosoma mansoni (Trematoda)

Abstract

BackgroundSchistosomiasis is a neglected tropical disease caused by trematodes of the genus Schistosoma. The pathogen is transmitted via freshwater snails. These snails indirectly benefit from agricultural pesticides which affect their enemy species. Pesticide exposure of surface waters may thus increase the risk of schistosomiasis transmission unless it also affects the pathogen. MethodologyWe tested the tolerance of the free-swimming infective life stages (miracidia and cercariae) of Schistosoma mansoni to the commonly applied insecticides diazinon and imidacloprid. Additionally, we investigated whether these pesticides decrease the ability of miracidia to infect and further develop as sporocysts within the host snail Biomphalaria pfeifferi. Principal findingsExposure to imidacloprid for 6 and 12 hours immobilized 50% of miracidia at 150 and 16 g/L, respectively (nominal EC50); 50% of cercariae were immobilized at 403 and 284 g/L. Diazinon immobilized 50% of miracidia at 51 and 21 g/L after 6 and 12 hours; 50% of cercariae were immobilized at 25 and 13 g/L. This insecticide tolerance is lower than those of the host snail B. pfeifferi but comparable to those of other commonly tested freshwater invertebrates. Exposure for up to 6 hours decreased the infectivity of miracidia at high sublethal concentrations (48.8 g imidacloprid/L and 10.5 g diazinon/L, i.e. 20 - 33 % of EC50) but not at lower concentrations commonly observed in the field (4.88 g imidacloprid/L and 1.05 g diazinon/L). The development of sporocysts within the snail host was not affected at any of these test concentrations. ConclusionsInsecticides did not affect the performance of S. mansoni at environmentally relevant concentrations. Accordingly, pesticide exposure is likely to increase the risk of schistosomiasis transmission by increasing host snail abundance without affecting the pathogen. Our results illustrate how the ecological side effects of pesticides are linked to human health, emphasizing the need for appropriate mitigation measures. Author summarySchistosomiasis is a major public health problem in 51 countries worldwide. Transmission requires human contact with freshwater snails that act as intermediate hosts, releasing free-swimming life stages of the trematodes. The host snails are highly tolerant to agricultural pesticides used in plant protection products. Pesticides enter freshwaters via drift and runoff, and indirectly foster the spread of host snails via adverse effects on more sensitive competitor and predator species in the water. Increasing the abundance of intermediate hosts raises potential contact with the human definitive host while transmission of the pathogen is not affected. Here we show that pesticides do not affect the ability of the trematode Schistosoma mansoni to infect and develop within its host snail Biomphalaria pfeifferi at environmentally relevant concentrations. Consequently, risk of schistosomiasis increases when pesticide pollution favours the proliferation of snail hosts whilst not negatively affecting the free-living parasites nor their development in their snail hosts. Measures to mitigate pesticide pollution of freshwaters should be a concern in public health programs to sustainably roll back schistosomiasis. Intersectional collaborations are required to bridge the gap between the agricultural and the public health sector in search of sustainable and safe methods of crop production.