The neonicotinoid imidacloprid impairs honey bee aversive learning of simulated predation

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 whether 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(-1)=20.8 ppb) over 4 days (mean of 1.5 ng per bee day(-1)), significantly impaired aversive short-term learning and memory retention. Imidacloprid treatment reduced short-term learning by 87% and memory retention by 85% in comparison with control 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 such as predator-prey relationships.