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Toxicological status changes the susceptibility of the honey bee Apis mellifera to a single fungicidal spray application

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Abstract

During all their life stages, bees are exposed to residual concentrations of pesticides, such as insecticides, herbicides, and fungicides, stored in beehive matrices. Fungicides are authorized for use during crop blooms because of their low acute toxicity to honey bees. Thus, a bee that might have been previously exposed to pesticides through contaminated food may be subjected to fungicide spraying when it initiates its first flight outside the hive. In this study, we assessed the effects of acute exposure to the fungicide in bees with different toxicological statuses. Three days after emergence, bees were subjected to chronic exposure to the insecticide imidacloprid and the herbicide glyphosate, either individually or in a binary mixture, at environmental concentrations of 0.01 and 0.1 μg/L in food (0.0083 and 0.083 μg/kg) for 30 days. Seven days after the beginning of chronic exposure to the pesticides (10 days after emergence), the bees were subjected to spraying with the fungicide difenoconazole at the registered field dosage. The results showed a delayed significant decrease in survival when honey bees were treated with the fungicide. Fungicide toxicity increased when honey bees were chronically exposed to glyphosate at the lowest concentration, decreased when they were exposed to imidacloprid, and did not significantly change when they were exposed to the binary mixture regardless of the concentration. Bees exposed to all of these pesticide combinations showed physiological disruptions, revealed by the modulation of several life history traits related mainly to metabolism, even when no effect of the other pesticides on fungicide toxicity was observed. These results show that the toxicity of active substances may be misestimated in the pesticide registration procedure, especially for fungicides.

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Acknowledgements

The authors would like to thank Jacques Sénéchal and Alexandre Gorit, who are beekeepers at the UR 406 INRAE Research Unit, for their expert beekeeping.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

This study was supported in part by recurrent funding from the Institut National de Recherche pour l’Agriculture, l’Alimentation et l'Environnement (INRAE) and by the Agence Nationale de la Recherche (ANR) (grant ANR-15-CE34-0004-01). Hanine Almasri was supported by grants from Lebanese University (grant number 2364) and the PACA region. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Conceptualization: Luc P. Belzunces and Jean-Luc Brunet; formal analysis: Hanine Almasri and Luc P. Belzunces; funding acquisition: Luc P. Belzunces; investigation: Hanine Almasri, Daiana Antonia Tavares, Deborah Sené, and Sylvie Tchamitchian; methodology: Hanine Almasri and Luc P. Belzunces; project administration: Luc P. Belzunces; resources: Sylvie Tchamitchian, Marianne Cousin, and Michel Pélissier; supervision: Luc P. Belzunces and Jean-Luc Brunet; visualization: Hanine Almasri and Luc P. Belzunces; writing — original draft: Hanine Almasri and Luc P. Belzunces; writing — review & editing: Luc P. Belzunces, Hanine Almasri, and Jean-Luc Brunet.

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Correspondence to Luc P. Belzunces.

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The authors declare no competing interests.

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Responsible Editor: Philippe Garrigues

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Almasri, H., Tavares, D.A., Tchamitchian, S. et al. Toxicological status changes the susceptibility of the honey bee Apis mellifera to a single fungicidal spray application. Environ Sci Pollut Res 28, 42807–42820 (2021). https://doi.org/10.1007/s11356-021-13747-3

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  • DOI: https://doi.org/10.1007/s11356-021-13747-3

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