Bumblebees socially learn behaviour too complex to innovate alone.

Culture refers to behaviours that are socially learned and persist within a population over time. Increasing evidence suggests that animal culture can, like human culture, be cumulative: characterized by sequential innovations that build on previous ones1. However, human cumulative culture involves behaviours so complex that they lie beyond the capacity of any individual to independently discover during their lifetime1-3. To our knowledge, no study has so far demonstrated this phenomenon in an invertebrate. Here we show that bumblebees can learn from trained demonstrator bees to open a novel two-step puzzle box to obtain food rewards, even though they fail to do so independently. Experimenters were unable to train demonstrator bees to perform the unrewarded first step without providing a temporary reward linked to this action, which was removed during later stages of training. However, a third of naive observer bees learned to open the two-step box from these demonstrators, without ever being rewarded after the first step. This suggests that social learning might permit the acquisition of behaviours too complex to 're-innovate' through individual learning. Furthermore, naive bees failed to open the box despite extended exposure for up to 24 days. This finding challenges a common opinion in the field: that the capacity to socially learn behaviours that cannot be innovated through individual trial and error is unique to humans.

Sub-cell scale features govern the placement of new cells by honeybees during comb construction.

Honeybee comb architecture and the manner of its construction have long been the subject of scientific curiosity. Comb is characterised by an even hexagonal layout and the sharing of cell bases and side walls, which provides maximised storage volume while requiring minimal wax. The efficiency of this structure relies on a regular layout and the correct positioning of cells relative to each other, with each new cell placed at the junction of two previously constructed cells. This task is complicated by the incomplete nature of cells at the edge of comb, where new cells are to be built. We presented bees with wax stimuli comprising shallow depressions and protuberances in simulation of features found within partially formed comb, and demonstrated that construction work by honeybee builders was influenced by these stimuli. The building of new cells was aligned to concave stimuli that simulated the clefts that naturally appear between two partially formed cells, revealing how new cells may be aligned to ensure proper tessellation within comb. We also found that bees built cell walls in response to edges formed by our stimuli, suggesting that cell and wall construction was specifically directed towards the locations necessary for continuation of hexagonal comb.

Bumblebees acquire alternative puzzle-box solutions via social learning.

The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees.

Animal Behaviour: Conformity and the Beginnings of Culture in an Insect.

Culture in animals is defined as socially learnt, group-specific behaviour, and has been found in many species. The discovery of social learning and cultural conformity in mate choice in Drosophila might allow for the investigation of the mechanistic underpinnings of gene-culture co-evolution.