Bumblebees socially learn behaviour too complex to innovate alone

The concept of animal culture, encompassing socially learned behaviors persisting within a population, is increasingly recognized. Cumulative culture, characterized by sequential innovations building upon previous ones, is particularly intriguing. While extensively documented in humans, where complexity exceeds individual capacity for independent discovery, evidence in invertebrates is lacking. This study investigates whether bumblebees, known for their social learning capabilities, can acquire a behavior too complex for individual innovation. The hypothesis is that a two-step puzzle box task, requiring an initially unrewarded action, would be insurmountable through individual learning but achievable via social learning. This research aims to test this hypothesis and explore the implications for understanding the evolution of complex behavior and cumulative culture.

Existing research suggests that animal culture, while less complex than human culture, can exhibit cumulative characteristics. Examples include changes in bird songs, humpback whale songs, and the sweet potato washing behavior of Japanese macaques, demonstrating cultural evolution and modifications over time. However, the extent of animal cultural evolution, particularly the capacity to learn behaviors beyond individual innovative capacity (a hallmark of human cumulative culture), remains debated. The 'ratchet effect', describing the retention and improvement of traditions, was believed to require higher-order social learning (imitative copying or teaching) considered uniquely human. However, studies like that involving pigeons finding more efficient routes collectively suggest that some animals might possess rudimentary cumulative culture, although the final behavior remains potentially attainable through individual learning. The crucial distinction lies in whether social learning allows acquisition of behaviors too complex for independent innovation within an individual's lifetime.

A novel two-step puzzle box was designed. To obtain a sucrose reward, bees had to first push a blue tab, then a red tab. Control experiments with two colonies (C1, C2 for 12 days, C3 for 24 days) exposed bees to the puzzle box without demonstrators, showing no independent learning. Demonstrator bees were trained using a staged reward system, initially rewarding both steps, then gradually removing the reward for the first step. Dyad experiments paired trained demonstrators with naive observer bees for 30-40 sessions (30-40 min each). Observers were subsequently tested in isolation to determine learning success. Two behavioral techniques were observed: 'staggered-pushing' and 'squeezing'. Following behavior, observers closely following demonstrators, was quantified. Post-learning solo foraging sessions assessed proficiency.

Control experiments revealed that bumblebees failed to solve the two-step puzzle box independently despite extended exposure (36-72 hours). In contrast, in dyad experiments, 5 out of 15 naive observer bees successfully learned the task from demonstrators, acquiring the complete behavior sequence without ever being rewarded for the first step. This suggests that bumblebees acquire behaviours socially that lie beyond their capacity for individual innovation. The success rate was influenced by the demonstrator's technique; all successful learners acquired the 'squeezing' technique, while none learned from demonstrators using 'staggered-pushing'. While the number of demonstrations did not correlate with learning success, a longer duration of 'following' behavior was observed in successful learners, especially those paired with 'squeezing' demonstrators. This suggests the importance of close observation during the learning process.

These findings provide the first evidence, to the authors' knowledge, of a non-human animal acquiring a behavior too complex for independent innovation through social learning. The bumblebees’ failure to solve the puzzle box independently, despite their capacity for innovation in simpler tasks, highlights the cognitive challenge posed by the unrewarded initial step and the temporal/spatial separation between actions and reward. The success of social learning, particularly with the 'squeezing' technique, suggests that combining actions into a single visually-guided movement facilitates learning. 'Following' behavior indicates that close observation might be crucial for efficient social learning. The results challenge the assumption of a fundamental cognitive divide between humans and animals regarding cumulative culture.

This study demonstrates that bumblebees can socially learn a behavior too complex for individual innovation, challenging long-held beliefs about the uniqueness of cumulative culture to humans. Future research should explore the broader implications of this finding for understanding cultural evolution across species, considering factors such as colony lifespan and environmental contexts which could limit the opportunity for cumulative cultural development in bumblebees, despite their demonstrable cognitive capacity.

The study's relatively small sample size might limit the generalizability of some findings, particularly those concerning the relationship between demonstrator technique and learning success. Additionally, the experimental setup, while novel, might not perfectly represent all aspects of natural bumblebee behavior and social learning. Further investigation is needed to determine the extent to which these findings generalize across other bumblebee species and under different environmental conditions. While the authors show that bumblebees are unlikely to solve the puzzle box independently, it cannot be entirely ruled out that an individual bee might be capable of solving it alone given an exceptionally long lifetime.