UC San Diego

Even at sublethal doses, neonicotinoids, commonly used insecticides can affect neurons involved in learning and memory, cognitive features that play a key role in colony fitness because they facilitate foraging. The commonly used neonicotinoid, imidacloprid, impairs the ability of bees to associate floral odors with a nectar reward. However, no studies, to date, have examined how if imidacloprid impairs negative associative learning. Sit- and-wait predators like spiders can attack foraging bees. Because bees can escape such attacks, learning to avoid dangerous foraging sites should enhance their survival. Negative associative learning classically uses electric shock as the punishing stimulus, although this is not natural. To better mimic predation, we developed a robo- predator so we consistently attack foragers with a pinching bite at a fixed force. Also, all prior aversive learning studies have used single, pure odors to test learning. We challenged bees with a more natural task and used the sting extension reflex (SER=the unconditioned response) to show that they can learn to associate an aversive biting stimulus with the complex odors of different Thymus vulgaris chemotypes. Bees exhibited a two fold higher SER response to the odors of punished as compared to non-punished chemotypes in short- and longer- term learning tests. Finally, we show that chronic exposure over 4 days to a sublethal concentration (25.56 [mu]g/L=20.79 ppb) significantly impairs negative short- term and longer-term learning. Control bees show 8 fold better short-term learning and longer-term learning than imidacloprid-treated bees. The impact of neonicotinoids on aversive learning and how bees avoid danger should therefore be more widely considered