Interactions Between Thiamethoxam and Deformed Wing Virus Can Drastically Impair Flight Behavior of Honey Bees.

Alberto Prado,Magali Ribière-Chabert,Eric Dubois,Marianne Coulon,Yves Le Conte,Richard Thiéry,Florine Arban,Cedric Alaux,Gennaro Di Prisco,Anne Dalmon

doi:10.3389/fmicb.2020.00766

Abstract

Exposure to multiple stress factors is believed to contribute to honey bee colony decline. However, little is known about how co-exposure to stress factors can alter the survival and behavior of free-living honey bees in colony conditions. We therefore studied the potential interaction between a neonicotinoid pesticide, thiamethoxam, and a highly prevalent honey bee pathogen, Deformed wing virus (DWV). For this purpose, tagged bees were exposed to DWV by feeding or injection, and/or to field-relevant doses of thiamethoxam, then left in colonies equipped with optical bee counters to monitor flight activity. DWV loads and the expression of immune genes were quantified. A reduction in vitellogenin expression level was observed in DWV-injected bees and was associated with precocious onset of foraging. Combined exposure to DWV and thiamethoxam did not result in higher DWV loads compared to bees only exposed to DWV, but induced precocious foraging, increased the risk of not returning to the hive after the first flight, and decreased survival when compared to single stress exposures. We therefore provided the first evidence for deleterious interactions between DWV and thiamethoxam in natural conditions.

Highlights

Heavy losses of honey bee colonies in the Northern hemisphere have been documented since the beginning of the 21st century (Lee et al, 2015)
Bees were kept overnight in an incubator at 34◦C with saturated humidity and 50% sucrose syrup. They were assigned to the following treatments: (1) control bees; (2) bees individually fed with 0.25 ng of thiamethoxam in 5 μl of syrup; (3) bees injected with PBS (Phosphate Buffer Saline solution); (4) bees injected with PBS and individually fed with 0.25 ng of thiamethoxam; (5) bees injected with Deformed wing virus (DWV) (∼104 copies/bee), and 6. bees injected with DWV (∼104 copies/bee) and individually fed with 0.25 ng of thiamethoxam
By co-exposing honey bees to DWV and thiamethoxam at environmentally relevant doses in their natural environment, we showed that the combination of both stressors caused premature foraging, a higher rate of failure to return to the colony and a steep decrease in survival

Summary

Introduction

Heavy losses of honey bee colonies in the Northern hemisphere have been documented since the beginning of the 21st century (Lee et al, 2015). There is a scientific consensus on the fact that honey bee colony losses are the result of multifactorial causes, including a decrease in floral resource availability, the spread of pathogens and pesticide use (Goulson et al, 2015). Honey bee colonies are frequently co-exposed to several pesticides and their corresponding metabolites, even when foraging in grasslands or non-agricultural areas (Hladik et al, 2016; Long and Krupke, 2016; Alburaki et al, 2018). Neonicotinoids have increasingly been used as insecticides for a wide range of crops for the past 20 years (Simon-Delso et al, 2015), which has resulted in frequent detection in honey bee hives (Lawrence et al, 2016) and hive products like honey (Jones and Turnbull, 2016; Mitchell et al, 2017). Despite EU policy measures for banning neonicotinoids they still persist in the environment (Wintermantel et al, 2020)

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