Sublethal effects of imidacloprid-contaminated honey stores on colony performance, queens, and worker activities in fall and early winter colonies

Authors: Carroll, Mark; Brown, Nicholas; Reitz, Dylan

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/20/2023
Publication Date: N/A
Citation: N/A

Interpretive Summary: Honey bees collect neonicotinoid insecticides in contaminated nectar which is then converted to honey stores where neonicotinoids persist. Bees exposed to very high levels of neonicotinoids may experience negative effects including reduced foraging, orientation, hygiene, mobility, queen egg-laying and stored sperm viability, brood rearing, and worker populations. Bees consume these contaminated sugar stores throughout the year, especially during dearth periods such as winter when outside floral nectar is very limited. We examined the effects of chronic neonicotinoid exposure on colony growth and performance, colony worker nutrition, and queen-worker interactions from early fall to mid-winter. Colonies were given the neonicotinoid imidacloprid in sugar syrup to simulate pesticide-contaminated nectars. Bee colonies received syrup containing 0 ppb (unexposed control), 20 ppb (moderately field relevant concentration), or 100 ppb (much higher than average field concentrations) imidacloprid over a from early September to mid-October to simulate collection of contaminated nectars from field flowers. Colonies were evaluated immediately before (pre-treatment), immediately after (post-treatment), and 10 weeks after this treatment period (mid-winter) to examine both immediate and delayed effects of dietary imidacloprid as colonies prepared for and entered winter. Significant negative effects were largely observed in colonies given 100 ppb imidacloprid syrup, which is a much higher concentration than observed in most agricultural crops. Post-treatment 100 ppb colonies had fewer adult workers than either 0 ppb colonies or 20 ppb colonies. Post-treatment 0 ppb colonies reared more brood than 20 ppb colonies or 100 ppb colonies while colonies from all treatments had similar amounts of stored pollen in their combs. Mid-winter 100 ppb colonies had much smaller adult worker populations, but not fewer stored pollen cells or brood, than 0 ppb or 20 ppb colonies. Close monitoring of individual adult workers tagged with RFID chips revealed that 100 ppb workers were less active over their adult lives in activities outside the colony such as foraging. RFID-tagged workers from different treatments had similar adult lifespans, but 100 ppb workers spent less time outside the colony than 0 ppb workers. Despite these treatment effects, adult workers from all treatments appeared to be sufficiently well fed as indicated by similar head protein levels at all time points. Imidacloprid exposure affected queen reproductive physiology (ovary nutrient stores), but not attraction of retinue workers (queen caretakers) or the queen pheromones that project her presence to the colony. Mid-winter 0 ppb queens had higher ovary proteins than 100 ppb queens and higher ovary lipids than 20 ppb queens. However, queen protein and lipid stores in a key non-reproductive tissue (fat body) did not differ across treatments. Queens from different treatment groups were attended by similar numbers of retinue workers and had similar levels of four QMP (Queen Mandibular Pheromone) compounds in their mandibular glands. These results suggest that honey bees are susceptible to high concentrations of imidacloprid both in newly collected nectar and later during winter in contaminated honey stores. This study also suggests that high levels of imidacloprid-contaminated sugar stores can negatively impact fall colony preparation for overwintering and winter colony performance.

Technical Abstract: Neonicotinoid-contaminated sugar stores can have both near term and long term effects on honey bees due to their persistence in honey stores. Lower Sonoran desert colonies were given treatment sugar syrups containing 0 ppb, 20 ppb (field relevant), or 100 ppb (above field relevant) imidacloprid over six weeks to simulate a contaminated early fall nectar flow. Colonies were evaluated immediately after (post-treatment) and 10 weeks after (mid-winter) the treatment phase to compare immediate and latent effects of neonicotinoid-contaminated sugar. During post-treatment evaluations, 0 ppb and 20 ppb colonies had larger adult populations than 100 ppb colonies and 0 ppb colonies had more brood than 20 ppb or 100 ppb colonies. Colonies experienced seasonal declines in stored pollen accumulation but no treatment effects. Lower colony performance among 100 ppb colonies was associated with reduced worker effort rather than adult lifespan. RFID tracking of individual workers revealed that workers from different treatment groups had similar adult lifespans; however, 100 ppb workers went outside the colony less often than 0 ppb workers. High levels of imidacloprid exposure affected queen but not worker nutritional physiology. Nest workers appeared to retain well-developed hypopharyngeal glands (as indicated by soluble head protein) across treatments and time points. Mid-winter queens from 0 ppb colonies had marginally higher ovary protein than queens from 100 ppb colonies and more ovary lipids than queens from 20 ppb colonies. Notably, however, queen nutrient stores in non-reproductive tissues (fat bodies) did not differ across treatment groups. Queens from different treatment groups were attended by comparable numbers of retinue workers and had similar mandibular gland contents of four QMP (Queen Mandibular Pheromone) components essential to queen retention and queen care. These results indicate that very high levels of imidacloprid exposure in nectar stores can negatively affect colony performance well after initial collection and storage.