Bumblebees acquire alternative puzzle-box solutions via social learning

Abstract

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.

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

“…Proficient learners from our single-step puzzle-box experiments typically attained proficiency over several days of foraging, and had access to boxes for 180 min each day for 6-12 days 18 . Thus, these comparatively low numbers are perhaps unsurprising.…”

“…Bumblebees were unable to solve the two-step puzzle box without a demonstrator. In our previous study, several bees successfully learned to open the two-option, single-step box under "control" open diffusion conditions, which were conducted in the absence of a trained demonstrator across 6-12 days 18 . Thus, to determine whether the two-step box could be solved individually, we sought to conduct a similar experiment.…”

“…Puzzle box. The two-step puzzle box was a modified version of the two-option puzzle box used in previous work by our group 18 . This incorporated a transparent lid that rotated anti-clockwise around a central axis when a red tab was pushed, exposing a 50% w/w sucrose solution reward on a yellow target; however, an additional blue tab initially blocked the path of the red tab (Fig.…”

Diversity of visual inputs to Kenyon cells of theDrosophilamushroom body

“…In particular, species of Hymenoptera, Lepidoptera, and Blattodea have evolved ~100-fold expansions of the mushroom body, and these expansions are correlated with increased visual input and striking visual learning abilities 9 . The increase in visual Kenyon cell number and microglomerular structures in there species 9,70-72 correlate with with visual learning abilities that surpass what has been observed in flies: Many hymenopterans and lepidopterans use visual navigation to forage and particular species have also been shown to count, to recognize the faces of individual conspecifics, to be able to learn based on observation and inference, and to recognize visual cue configuration and abstraction 70,[73][74][75][76][77][78][79][80][81][82][83][84][85][86] . However, the lack of genetic control in these species means a requirement for the mushroom body in visual learning has been addressed only rarely 15,[44][45][46] .…”

Competition and generalization impede cultural formation in wild jackdaws

“…One commonly used approach is diffusion experiments, where novel information or behaviour is seeded into a naive population by 'demonstrators' that have typically been trained on one of two equal-pay-off options [8][9][10][11][12][13]. This approach provides important benefits in terms of experimental control and interpretability [9] and has been vital in demonstrating that animal culture can arise through social learning [8,10,14], but it may not necessarily reflect conditions found in the wild. The seeding of demonstrators with strong preferences, alongside the use of paradigms that reduce the effects of competition and limit the scope for generalization, may inadvertently produce conditions that are particularly conducive to the establishment of cultures.…”