Neonicotinoid pesticides dinotefuran increase honeybee body temperature and accelerate honeybee (Apis mellifera) translocation of contaminants into hives to enhance ecotoxicity risk

Neonicotinoid pesticides are strongly believed to exhibit a higher risk of ecotoxicity to honeybee populations. However, the underlying reasons have not been clarified. Our research indicates that neonicotinoid pesticides dinotefuran affected acetylcholine receptors, which led to an elevation in octopamine titer and subsequent increase in the body temperature of honeybees. Furthermore, we observed a considerable upregulation the expression of a flight gene flightin in honeybees. This gene accelerates the homing behavior of honeybees and facilitates the rapid and frequent transport of neonicotinoid pesticide-contaminated nectar to the hive. Consequently, this accelerated the enrichment of neonicotinoid pesticides and increased the toxicity risk to the honeybee population. Stereochiral configuration S -dinotefuran exhibited a markedly higher influence on the body temperature of honeybees and the expression of flight genes than R -dinotefuran. The transcriptomic data further demonstrated that S -dinotefuran and R -dinotefuran influenced the thermogenesis, glycolytic, mitochondrial metabolism, and other energy metabolic pathways. We propose for the first time that neonicotinoid pesticides accelerate the homing of honeybees, which in turn hastens the transfer of neonicotinoid pesticides into their hives. This phenomenon may explain the frequent appearance and higher concentrations of neonicotinoid pesticides residual in the hive and one of the reasons why these pesticides are more ecotoxicity than others. • Dinotefuran disrupts octopamine titers and thermogenesis, elevating honeybee body temperature. • Dinotefuran upregulate flight genes, accelerating honeybee homing. • Honeybees transfer more dinotefuran into nests and elevating ecological risk.