The direct and indirect effects of environmental toxicants on the health of bumble bees and their microbiomes

Abstract

Bumble bees (Bombus spp.) are important and widespread insect pollinators, but the act of foraging on flowers can expose them to harmful pesticides and chemicals such as oxidizers and heavy metals. How these compounds directly influence bee survival and indirectly affect bee health via the gut microbiome is largely unknown. As toxicants in floral nectar and pollen take many forms, we explored the genomes of bee-associated microbes for their potential to detoxify cadmium, copper, selenate, the neonicotinoid pesticide imidacloprid, and hydrogen peroxide - which have all been identified in floral nectar and pollen. We then exposed Bombus impatiens workers to varying concentrations of these chemicals via their diet and assayed direct effects on bee survival. Using field-realistic doses, we further explored indirect effects on bee microbiomes. We found multiple putative genes in core gut microbes that may aid in detoxifying harmful chemicals. We also found that while the chemicals are largely toxic at levels within and above field-realistic concentrations, the field-realistic concentrations - except for imidacloprid - altered the composition of the bee microbiome, potentially causing gut dysbiosis. Overall, our study shows that chemicals found in floral nectar and pollen can cause bee mortality, and likely have indirect, deleterious effects on bee health via their influence on the bee microbiome.

Bumble bees (Bombus spp.) are important and widespread insect pollinators, but the act of foraging on flowers can expose them to harmful pesticides and chemicals such as oxidizers and heavy metals. How these compounds directly influence bee survival and indirectly affect bee health via the gut microbiome is largely unknown. As toxicants in floral nectar and pollen take many forms, we explored the genomes of bee-associated microbes for their potential to detoxify cadmium, copper, selenate, the neonicotinoid pesticide imidacloprid, and hydrogen peroxide - which have all been identified in floral nectar and pollen. We then exposed Bombus impatiens workers to varying concentrations of these chemicals via their diet and assayed direct effects on bee survival. Using field-realistic doses, we further explored indirect effects on bee microbiomes. We found multiple putative genes in core gut microbes that may aid in detoxifying harmful chemicals. We also found that while the chemicals are largely toxic at levels within and above field-realistic concentrations, the field-realistic concentrations - except for imidacloprid - altered the composition of the bee microbiome, potentially causing gut dysbiosis. Overall, our study shows that chemicals found in floral nectar and pollen can cause bee mortality, and likely have indirect, deleterious effects on bee health via their influence on the bee microbiome.