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 environmental 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 the toxins and toxicants in floral nectar and pollen take many forms, we explored the genomes of core bumblebee microbes (Using RAST) for their potential to detoxify cadmium, copper, selenium, 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 spiked into their diet and identified the direct effects on bee survival. Using field realistic doses, we further explored indirect effects on bee microbiomes. We found multiple genes in core gut microbes that have the potential to 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 environmental chemicals found in floral nectar and pollen can directly cause bee mortality, and at field-realistic levels, likely have indirect, deleterious effects on bee health via their influence on the bee microbiome.

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

“…Lastly, we tested our beta diversity data for statistical significance in R v3.5.1 with the packages 'vegan' [54] and 'DESeq2' [55]. Data and representative code can be found on Data Dryad (doi:10.7280/D14T2K) and a preprint of this study was posted to the bioRxiv [56].…”

Impacts of multiple pollutants on pollinator activity in road verges

“…of Zn between 55 and 1,158 ppm (a similar range to that measured in road verge flowers) have been found to affect caterpillar survival and development (Shephard et al, 2020). A recent study estimated that the LC50 after 7 days for bumblebees feeding on contaminated sugar water was 0.83 ppm for Cd and 66.55 ppm for Cu (Rothman et al, 2020). These are comparable to some of the highest concentrations that we measured, though a study on honeybees found that the LC50 was far greater than roadside-realistic concentrations for Cd and Pb (Di et al, 2016).…”

“…Further research is needed to understand if and how this might affect them, though concentrations of Pb have been negatively related to bumblebee colony growth in urban areas (Sivakoff et al., 2020), concentrations of Cd, Pb and Zn have been linked to wild bee abundance, diversity and forewing structure (Moroń et al., 2012; Szentgyörgyi et al., 2017) and concentrations of Zn between 55 and 1,158 ppm (a similar range to that measured in road verge flowers) have been found to affect caterpillar survival and development (Shephard et al., 2020). A recent study estimated that the LC50 after 7 days for bumblebees feeding on contaminated sugar water was 0.83 ppm for Cd and 66.55 ppm for Cu (Rothman et al., 2020). These are comparable to some of the highest concentrations that we measured, though a study on honeybees found that the LC50 was far greater than roadside‐realistic concentrations for Cd and Pb (Di et al., 2016).…”

“…Urbini et al., 2006; Zhou et al., 2018). Many metals are toxic to insects at sufficient concentrations (Di et al., 2016; Muñoz et al., 2015; Rothman et al., 2020), and they might affect the attractiveness of floral resources at much lower levels. Moroń et al.…”

Social Interaction is Unnecessary for Hindgut Microbiome Transmission in Honey Bees: the Effect of Diet and Social Exposure on Tissue-Specific Microbiome Assembly

“…Confirming earlier hypotheses [68], the significant abundance of established G. apicola variants relative to the other core members suggests that the early ileum ecosystem and/or S. alvi specifically selects for G. apicola diversity of function (Table 1). Correspondingly, G. apicola strains show notable variation across many functional categories including oxidative stress and carbohydrate utilization, while S. alvi strains are typically fixed for similar functions indicating competition and host fidelity respectively [38,48,[71][72][73].…”