Cognitive effects of chlorantraniliprole alone or in mixture with a pyrethroid in honey bees

Chlorantraniliprole is a diamide insecticide targeting insect ryanodine receptors, which are involved in intracellular calcium release in neurons and muscles. In turn, this calcium release triggers neurotransmitter exocytosis and muscle contraction. Despite the presence of these receptors within neurons, possible effects of this insecticide on cognitive function have not been addressed yet. Honey bees are vital pollinators and serve as a valuable model for studying insect cognition, through the use of appetitive learning. Here, we assessed the sublethal effects of chlorantraniliprole on bees' olfactory perception, learning and memory. Given that bees are exposed to multiple pesticides while foraging, we examined the effect of chlorantraniliprole alone or in combination with a pyrethroid insecticide to determine potential cocktail effects on cognition. To this aim, we used the conditioning of the proboscis extension response (PER) and assessed the effect of pesticide exposure on several aspects of bee cognition. Non-associative learning was assessed through habituation of the PER, while associative learning and olfactory generalization were assessed using absolute conditioning. Finally, bees' olfactory discrimination abilities were measured through differential conditioning of the PER. Chlorantraniliprole was found to strongly affect bees' habituation and olfactory discrimination performances. Both antagonist and additive cocktail effects were found using both pesticides together. These results indicate that low-dose chlorantraniliprole contamination may negatively impact bees' ability to find fruitful floral sources while foraging, and in turn impair their pollination service.