Agricultural pesticides do not suppress infection ofBiomphalaria(Gastropoda) bySchistosoma mansoni(Trematoda)
Authors: Ganatra Akbar A. , Becker Jeremias M. , Shahid Naeem , Kaneno Salim , Hollert Henner , Liess Matthias , Agola Eric L. , McOdimba Francis , Fillinger Ulrike 
Published: February 2023

Background

Schistosomiasis is a neglected tropical disease caused by trematodes of the genusSchistosoma. 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.

Methodology

We tested the tolerance of the free-swimming infective life stages (miracidia and cercariae) ofSchistosoma mansonito 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 snailBiomphalaria pfeifferi.

Principal findings

Exposure to imidacloprid for 6 and 12 hours immobilized 50% of miracidia at 150 and 16 μg/L, respectively (nominal EC50); 50% of cercariae were immobilized at 403 and 284 μg/L. Diazinon immobilized 50% of miracidia at 51 and 21 μg/L after 6 and 12 hours; 50% of cercariae were immobilized at 25 and 13 μg/L. This insecticide tolerance is lower than those of the host snailB. pfeifferibut 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 μg imidacloprid/L and 10.5 μg diazinon/L, i.e. 20 - 33 % of EC50) but not at lower concentrations commonly observed in the field (4.88 μg imidacloprid/L and 1.05 μg diazinon/L). The development of sporocysts within the snail host was not affected at any of these test concentrations.

Conclusions

Insecticides did not affect the performance ofS. mansoniat 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 summary

Schistosomiasis 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 trematodeSchistosoma mansonito infect and develop within its host snailBiomphalaria pfeifferiat 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.