A neonicotinoid, imidacloprid, impairs honey bee aversive learning of simulated predation

Abstract

Neonicotinoid insecticides can impair bee learning and memory, cognitive features that play a key role in colony fitness because they facilitate foraging. For example, the commonly used neonicotinoid, imidacloprid, reduces honey bee olfactory learning. However, no studies have previously determined if imidacloprid can impair aversive associative learning, although such learning should enhance bee survival by allowing bees to avoid dangerous foraging sites. To mimic attempted predation of foragers, we developed an electro-mechanical predator that consistently attacked foragers with a pinching bite at a fixed force and elicited aversive olfactory learning in a sting extension response (SER) assay. We show that chronic exposure to a sublethal concentration of imidacloprid (25.6 μg/L=20.8 ppb) over 4 days (mean of 1.5 μg/bee/day), significantly impaired aversive short-term learning and memory retention. Control bees showed 9-10 fold higher short-term learning and 8-fold higher memory retention (1 hr later) than imidacloprid-treated bees. Imidacloprid therefore impairs the ability of honey bees to associate a naturalistic predation stimulus, biting, with floral odor compounds. Such learning should enhance bee survival, suggesting that xenobiotics could alter more complex ecological interactions like predator-prey relationships.