Imidacloprid Decreases Honey Bee Survival Rates but Does Not Affect the Gut Microbiome

Abstract

Accumulating evidence suggests that pesticides have played a role in the increased rate of honey bee colony loss. One of the most commonly used pesticides in the United States is the neonicotinoid imidacloprid. Although the primary mode of action of imidacloprid is on the insect nervous system, it has also been shown to cause changes in insects' digestive physiology and alter the microbiota of larvae. The honey bee gut microbiome plays a major role in bee health. Although many studies have shown that imidacloprid affects honey bee behavior, its impact on the microbiome has not been fully elucidated. Here, we investigated the impact of imidacloprid on the gut microbiome composition, survivorship, and susceptibility to pathogens of honey bees. Consistent with other studies, we show that imidacloprid exposure results in an elevated mortality of honey bees in the hive and increases the susceptibility to infection by pathogens. However, we did not find evidence that imidacloprid affects the gut bacterial community of honey bees. Our experiments demonstrated that honey bee gut bacteria can grow in the presence of imidacloprid, and we found some evidence that imidacloprid can be metabolized in the bee gut environment. However, none of the individual bee gut bacterial species tested could metabolize imidacloprid, suggesting that the observed metabolism of imidacloprid within bee gut cultures is not caused by the gut bacteria. Overall, our results indicate that imidacloprid causes increased mortality in honey bees, but this mortality does not appear to be linked to the microbiome. Growing evidence suggests that the extensive use of pesticides has played a large role in the increased rate of honey bee colony loss. Despite extensive research on the effects of imidacloprid on honey bees, it is still unknown whether it impacts the community structure of the gut microbiome. Here, we investigated the impact of imidacloprid on the gut microbiome composition, survivorship, and susceptibility to pathogens of honey bees. We found that the exposure to imidacloprid resulted in an elevated mortality of honey bees and increased the susceptibility to infection by opportunistic pathogens. However, we did not find evidence that imidacloprid affects the gut microbiome of honey bees. We found some evidence that imidacloprid can be metabolized in the bee gut environment , but because it is quickly eliminated from the bee, it is unlikely that this metabolism occurs in nature. Thus, imidacloprid causes increased mortality in honey bees, but this does not appear to be linked to the microbiome.

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

“…Imidacloprid did not affect the diversity of the gut microbiome in B. impatiens whatsoever. These results agree with a previous experiment that showed imidacloprid did not affect the honey bee microbial community, and that bee gut bacteria do not appear to metabolize the neurotoxicant (48). As imidacloprid targets acetylcholine receptors in insects (103) it is perhaps not surprising that the bumble bee gut microbiome is not affected by this insecticide.…”

“…Furthermore, there are individual ESVs of symbiotic or pathogenic bacteria that are tolerant or susceptible to most of these chemicals. Previous studies have examined whether the microbiome is affected by our assayed poisons in several non-bee species (42–47) and in honey bees and bumble bees (22,48,53). We extend this work by screening a broad panel of toxicants on bees and their symbionts, and further show that members of the bee microbiota vary in their tolerance to the chemicals.…”

“…Cadmium (42,43), selenium (44), copper (45), imidacloprid (46), and hydrogen peroxide (as measured as ROS (47)) have been shown to alter host microbiomes in non-bee study systems. Outside of our work, little is known about how these toxicants affect bee microbiota, with field-realistic selenium and cadmium exposure altering proportions of microbes in honey bees (22), and imidacloprid not affecting the microbiome of honey bees (48). While the effects of toxicants on host-associated microbes have been studied in many systems, a new paradigm is emerging in which the microbiome potentially protects its host from metal(loid) toxicity.…”

The bumble bee microbiome increases survival of bees exposed to selenate toxicity

“…We note that these bacteria grew somewhat poorly, indicating that our culturing conditions are not optimal for bee symbionts. Similar OD readings, however, have been reported in other studies using different strains of these bacteria (Raymann et al, 2018).…”

“…This conflicting result may be due to the compositional nature of microbiome data (Gloor et al, ) in which other changes in proportional abundance may not reflect changes in absolute abundance. Likewise, these bacteria grew poorly in culture, which may mask the true effects of dose‐dependent selenate exposure as an artefact, although strains of S. alvi and other Firm‐5 lactobacilli have grown to similar OD 600 readings in the previous studies (Raymann et al, ). We also cannot examine genomic differences between cultured strains and taxa identified in our bee samples as we are unable to discern their entire genomes from a 16S rRNA gene sequencing survey.…”