Abstract

Neonicotinoid insecticides have been implicated in the rapid global decline of bumblebees over recent years, particularly in agricultural and urban areas. While there is much known about neonicotinoid toxicity effects at the colony stage of the bumblebee annual cycle, far less is known about such effects at other stages critical for the maintenance of wild populations. In the present work, individual-based feeding assays were used to show that chronic consumption of the widely used neonicotinoid clothianidin at a field-realistic average rate of 3.6 and 4.0 ng/g·bee/day reduces survival of queen and male bumblebees, respectively, within a 7-day period. In contrast, worker survival was unaffected at a similar consumption rate of 3.9 ng/g·bee/day. To test the hypothesis that males have a lower tolerance for oral clothianidin exposure than workers due to their haploid genetic status, RNAseq analysis was used to compare the transcriptomic responses of workers and males to chronic intake of clothianidin at a sub-lethal dose of 0.37ng/bee/day for 5 days. Surprisingly, clothianidin consumption only altered the expression of 19 putative detoxification genes in a sex-specific manner, with 11/19 genes showing increased expression in workers. Sub-lethal clothianidin exposure also altered the expression of 40 genes associated with other major biological functions, including locomotion, reproduction, and immunity. Collectively, these results suggest that chronic oral toxicity effects of neonicotinoids are greatest during mating and nest establishment phases of the bumblebee life cycle. Chronic oral toxicity testing on males and queens is therefore required in order to fully assess the impact of neonicotinoids on wild bumblebee populations.

Highlights

  • Bumblebees have rapidly declined in abundance, species richness, and geographic distribution on a global scale over recent years [1, 2]

  • Chronic oral toxicity effects of clothianidin differ among queen, worker, and male bumblebees

  • The present study shows that chronic consumption of field-realistic doses of the widely used neonicotinoid pesticide clothianidin has differential effects on the survival of queen, worker, and male bumblebees

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Summary

Introduction

Bumblebees have rapidly declined in abundance, species richness, and geographic distribution on a global scale over recent years [1, 2]. Effect of chronic oral neonicotinoid exposure on bumblebee health which was recently listed as an endangered species by the U.S Fish and Wildlife Service. These declines pose a significant threat to the function and diversity of temperate ecosystems due to the critical keystone role that bumblebees play as pollinators of native flowering plants. Reports of parallel reductions in bee-pollinated plant species suggest that pollinator decline-mediated effects on wildlife diversity at higher trophic levels may already be well underway [1, 6, 7]. It is imperative that all anthropogenic stressors contributing to species decline in bumblebees be identified and mitigated as soon as possible

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