Exposure to field-realistic levels of flupyradifurone and thiamethoxam reduces nursing behavior and accelerates foraging onset in Apis mellifera.

Honey bees are essential pollinators in agricultural and natural ecosystems. As a eusocial insect, the honey bee colony is composed of individuals performing different tasks according to their age-dependent caste, with younger nurses caring for the brood and older foragers collecting food outside the hive. Recently, insecticide-induced disruptions in this division of labor have been implicated as factors contributing to colony collapse, but the behavioral and physiological effects of insecticides on nurses remain poorly understood. We investigated the effects of two nicotinic acetylcholine receptor-agonistic insecticides, flupyradifurone (FPF) and thiamethoxam (THX), on brood-caring behavior and caste-differentiation-related gene expression in nurse bees at field-realistic residue levels under controlled laboratory conditions. Both insecticides decreased nursing behavior and shifted expression of selected genes toward a forager-like profile. In particular, both methyl farnesoate epoxidase and tyramine β-hydroxylase, genes involved in juvenile hormone and octopamine synthesis, respectively, and known to promote the nurse-to-forager transition, were upregulated. Additionally, we analyzed foraging parameters (foraging onset, duration, and total and daily foraging counts) at the colony level using a radio frequency identification system under field conditions. Both insecticides accelerated the onset of foraging, with FPF increasing total foraging trips and THX reducing survival, while other foraging parameters were largely unaffected. Our findings provide the first integrative evidence that these two insecticides disrupt task allocation and task performance in both nurses and foragers. This indicates that exposure to even field-realistic residue levels can jeopardize colony stability, underscoring the need for more precautionary use of these compounds and stronger regulation.