Social learning of a challenging two-step action sequence fulfils key criteria of cumulative culture in an insect

Abstract

Culture in non-human animals refers to behaviour that is socially learned and persists within a population over time. Human culture is notable in that it is cumulative: new innovations have built on previous ones over thousands of years. As a result, what is acquired via social learning often goes far beyond the capacity of any individual to independently discover it during their lifetime1-3. To date, no previous study has convincingly demonstrated this phenomenon in a non-human animal. Here, we show that bumblebees can learn from a trained demonstrator to open a novel, 3D-printed two-step puzzle box to obtain food rewards, even though they fail to do so independently. Experimenters were unable to train demonstrators to perform the unrewarded first step of the behaviour without providing a temporary reward linked to this action: the reward then being removed during later stages of training. However, a third of naive observers learned to open the two-step box from these demonstrators, without ever having been rewarded after the first step. This suggested that social learning might permit the acquisition of behaviours too complex to "re-innovate" via individual learning. Furthermore, naive bees failed to open the box despite extended exposure over the course of 12 days. The temporal and spatial distance of the unrewarded first step from the reward appeared to inhibit acquisition of two-step box-opening via individual associative learning, but this limitation was overcome by the presence of a trained conspecific. To our knowledge, these results make bumblebees the first animal to demonstrate the ability to socially learn a behaviour that is beyond their ability to innovate individually. This finding challenges the prevailing opinion of the field, which generally considers cumulative culture, which is built on this capacity, to be unique to humans.