Physiological effects of the interaction between Nosema ceranae and sequential and overlapping exposure to glyphosate and difenoconazole in the honey bee Apis mellifera

Hanine Almasri,Maryline Pioz,Marianne Cousin,Daiana Antonia Tavares,Marie Diogon,Jean-Luc Brunet,Luc P. Belzunces,Sylvie Tchamitchian,Maryam Alamil,Déborah Sené

doi:10.1016/j.ecoenv.2021.112258

Abstract

Pathogens and pollutants, such as pesticides, are potential stressors to all living organisms, including honey bees. Herbicides and fungicides are among the most prevalent pesticides in beehive matrices, and their interaction with Nosema ceranae is not well understood. In this study, the interactions between N. ceranae, the herbicide glyphosate and the fungicide difenoconazole were studied under combined sequential and overlapping exposure to the pesticides at a concentration of 0.1 µg/L in food. In the sequential exposure experiment, newly emerged bees were exposed to the herbicide from day 3 to day 13 after emerging and to the fungicide from day 13 to day 23. In the overlapping exposure experiment, bees were exposed to the herbicide from day 3 to day 13 and to the fungicide from day 7 to day 17. Infection by Nosema in early adult life stages (a few hours post emergence) greatly affected the survival of honey bees and elicited much higher mortality than was induced by pesticides either alone or in combination. Overlapping exposure to both pesticides induced higher mortality than was caused by sequential or individual exposure. Overlapping, but not sequential, exposure to pesticides synergistically increased the adverse effect of N. ceranae on honey bee longevity. The combination of Nosema and pesticides had a strong impact on physiological markers of the nervous system, detoxification, antioxidant defenses and social immunity of honey bees.

Highlights

All living organisms are subjected to multiple stressors from anthropogenic and natural sources (Holmstrup et al, 2010)
The effects of the sequence of exposure to pesticides on honey bee survival were assessed in both bees infected with Nosema and uninfected bees (Fig. 2 and Table S1)
Under overlapping exposure, difenoconazole may enhance the toxicity of glyphosate by inhibiting its metabolism, which is less likely under sequential exposure

Summary

Introduction

All living organisms are subjected to multiple stressors from anthropogenic (e.g., pollutants) and natural (e.g., pathogens) sources (Holmstrup et al, 2010). Honey bees could be subjected to simultaneous, sequential or overlapping exposure to pesticides that can elicit additive and synergistic adverse effects (Gill, 2012; Sgolastra, 2017; Zhu, 2017). Simultaneous exposure occurs via the ingestion of food contaminated by several pesticides, by contact with plant parts contaminated with different pesticide residues or during plant treatment with a mixture of pesticides. Sequential and overlapping exposure may be observed when consecutive treatments are applied to a crop, when bees visit different crops during foraging, when a migratory beekeeping strategy is applied, when bees consume honey or pollen successively contaminated with different pesticides or when bees are exposed to pesticides outside the hive after consuming contaminated food (Luttik et al, 2017)

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