Complex operant learning by worker bumblebees (Bombus impatiens): detour behaviour and use of colours as discriminative stimuli

Abstract

Animals react to salient stimuli via unconditioned responses, Pavlovian conditioning, conditioned manipulation of objects in simple and complex ways (instrumental/operant learning and tool use) and insight learning. Bumblebees are known to learn to manipulate natural and artificial complex flowers to obtain rewards. Even though those tasks involve instrumental learning, all have been rather natural, resembling activities that bees would perform living free in the wild. None have involved the generation of more unnatural, arbitrary responses (true operants) such as detour behaviour; in which subjects have to gain a completely hidden, covered reward by moving objects away from it by multiple body lengths. Furthermore, few have involved discriminative stimuli, wherein subjects learn that the appropriate way to perform an operant is signalled by specific cues. We therefore trained bumblebees with two types of task that we believe represented challenges unlike any they have evolved to respond to. These involved dragging various-sized caps aside and rotating discs through varying arcs away from the entrances of artificial flowers (via detours of up to three body lengths), to access a reward hidden beneath. Further, we successfully trained bees to use disc colour as a discriminative stimulus predicting whether rotating discs clockwise or counterclockwise would reveal the reward. This true, complex operant conditioning demonstrated that bumblebees can learn novel, arbitrary behavioural sequences, manipulating and moving items in ways that seem far from any natural task that they would encounter, and doing so flexibly in response to specific discriminative stimuli. This adds to growing evidence of impressive behavioural plasticity and learning abilities in bees, and suggests new approaches for probing their cognitive abilities in the future.