Bumblebees attend to both the properties of the string and the target in string-pulling tasks, but prioritize the features of the string.

Previous studies have demonstrated that associative learning and experience play important roles in the string-pulling of bumblebees (Bombus terrestris). However, the features of the target (artificial flower with sugar reward) and the string that bees learn in such tasks remain unknown. This study aimed to explore the specific aspects of the string-flower arrangement that bumblebees learn and how they prioritize these features. We show that bumblebees trained with string-pulling are sensitive to the flower stimuli; they exhibit a preference for pulling strings connected to flowers over strings that are not attached to a target. Additionally, they chose to pull strings attached to flowers of the same color and shape as experienced during training. The string feature also plays a crucial role for bumblebees when the flower features are identical. Furthermore, bees prioritized the features of the strings rather than the flowers when both cues were in conflict. Our results show that bumblebees solve string-pulling tasks by acquiring knowledge about the characteristics of both targets and strings, and contribute to a deeper understanding of the cognitive processes employed by bees when tackling non-natural skills.

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.

Is it time for insect researchers to consider their subjects' welfare?

Recent evidence suggests that at least some insect species might plausibly feel pain. These findings should prompt researchers to think about the welfare implications of insect experiments.

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.

Bees learn to dance.

Experience yields precision in the waggle dance of honey bees.

Bumblebees retrieve only the ordinal ranking of foraging options when comparing memories obtained in distinct settings.

Are animals' preferences determined by absolute memories for options (e.g. reward sizes) or by their remembered ranking (better/worse)? The only studies examining this question suggest humans and starlings utilise memories for both absolute and relative information. We show that bumblebees' learned preferences are based only on memories of ordinal comparisons. A series of experiments showed that after learning to discriminate pairs of different flowers by sucrose concentration, bumblebees preferred flowers (in novel pairings) with (1) higher ranking over equal absolute reward, (2) higher ranking over higher absolute reward, and (3) identical qualitative ranking but different quantitative ranking equally. Bumblebees used absolute information in order to rank different flowers. However, additional experiments revealed that, even when ranking information was absent (i.e. bees learned one flower at a time), memories for absolute information were lost or could no longer be retrieved after at most 1 hr. Our results illuminate a divergent mechanism for bees (compared to starlings and humans) of learned preferences that may have arisen from different adaptations to their natural environment.

Descending control of nociception in insects?

Modulation of nociception allows animals to optimize chances of survival by adapting their behaviour in different contexts. In mammals, this is executed by neurons from the brain and is referred to as the descending control of nociception. Whether insects have such control, or the neural circuits allowing it, has rarely been explored. Based on behavioural, neuroscientific and molecular evidence, we argue that insects probably have descending controls for nociception. Behavioural work shows that insects can modulate nocifensive behaviour. Such modulation is at least in part controlled by the central nervous system since the information mediating such prioritization is processed by the brain. Central nervous system control of nociception is further supported by neuroanatomical and neurobiological evidence showing that the insect brain can facilitate or suppress nocifensive behaviour, and by molecular studies revealing pathways involved in the inhibition of nocifensive behaviour both peripherally and centrally. Insects lack the endogenous opioid peptides and their receptors that contribute to mammalian descending nociception controls, so we discuss likely alternative molecular mechanisms for the insect descending nociception controls. We discuss what the existence of descending control of nociception in insects may reveal about pain perception in insects and finally consider the ethical implications of these novel findings.

Motivational trade-offs and modulation of nociception in bumblebees.

Insects are traditionally thought to respond to noxious stimuli in an inflexible manner, without the ability to modulate their behavior according to context. We investigated whether bumblebees' attraction to high sucrose solution concentrations reduces their avoidance of noxious heat. Bees were given the choice between either unheated or noxiously heated (55 °C) feeders with different sucrose concentrations and marked by different colors. Bees avoided noxious feeders when the unheated feeders contained high sucrose concentrations, but progressively increased feeding from noxious feeders when the sucrose concentration at unheated feeders decreased. This shows a motivational trade-off of nociceptive responses. Bees used learned color cues for their decisions, and thus the trade-off was based on processing in the brain, rather than just peripheral processing. Therefore, bees can use contextual information to modulate nociceptive behavior. This ability is consistent with a capacity for pain experiences in insects.

Discrimination of edge orientation by bumblebees.

Simple feature detectors in the visual system, such as edge-detectors, are likely to underlie even the most complex visual processing, so understanding the limits of these systems is crucial for a fuller understanding of visual processing. We investigated the ability of bumblebees (Bombus terrestris) to discriminate between differently angled edges. In a multiple-choice, "meadow-like" scenario, bumblebees successfully discriminated between angled bars with 7° differences, significantly exceeding the previously reported performance of eastern honeybees (Apis cerana, limit: 15°). Neither the rate at which bees learned, nor their final discrimination performance were affected by the angular orientation of the training bars, indicating a uniform performance across the visual field. Previous work has found that, in dual-choice tests, eastern honeybees cannot reliably discriminate between angles with less than 25° difference, suggesting that performance in discrimination tasks is affected by the training regime, and doesn't simply reflect the perceptual limitations of the visual system. We used high resolution LCD monitors to investigate bumblebees' angular resolution in a dual-choice experiment. Bumblebees could still discriminate 7° angle differences under such conditions (exceeding the previously reported limit for Apis mellifera, of 10°, as well as that of A. cerana). Bees eventually reached similar levels of accuracy in the dual-choice experiment as they did under multiple-choice conditions but required longer learning periods. Bumblebees show impressive abilities to discriminate between angled edges, performing better than two previously tested species of honeybee. This high performance may, in turn, support complex visual processing in the bumblebee brain.

Social cognition in insects.

Insects feature some of the most complex societies in the animal kingdom, but a historic perception persists that such complexity emerges from interactions between individuals whose behaviours are largely guided by innate routines. Challenging this perception, recent work shows that insects feature many aspects of social intelligence found in vertebrate societies, such as individual recognition, learning object manipulation by observation, and elements of cultural traditions. Insects also display emotion-like states, which may be linked to social behaviours such as rescuing others from danger. We review recent developments in insect social cognition and speculate that some forms of now-hardwired behaviour (e.g., nest construction) could have initially been the result of individual innovation and subsequent cultural spread, with evolution later cementing these behaviours into innate behaviour routines.

Genomic Signatures of Recent Adaptation in a Wild Bumblebee.

Environmental changes threaten insect pollinators, creating risks for agriculture and ecosystem stability. Despite their importance, we know little about how wild insects respond to environmental pressures. To understand the genomic bases of adaptation in an ecologically important pollinator, we analyzed genomes of Bombus terrestris bumblebees collected across Great Britain. We reveal extensive genetic diversity within this population, and strong signatures of recent adaptation throughout the genome affecting key processes including neurobiology and wing development. We also discover unusual features of the genome, including a region containing 53 genes that lacks genetic diversity in many bee species, and a horizontal gene transfer from a Wolbachia bacteria. Overall, the genetic diversity we observe and how it is distributed throughout the genome and the population should support the resilience of this important pollinator species to ongoing and future selective pressures. Applying our approach to more species should help understand how they can differ in their adaptive potential, and to develop conservation strategies for those most at risk.

Gut microbiome drives individual memory variation in bumblebees.

The potential of the gut microbiome as a driver of individual cognitive differences in natural populations of animals remains unexplored. Here, using metagenomic sequencing of individual bumblebee hindguts, we find a positive correlation between the abundance of Lactobacillus Firm-5 cluster and memory retention on a visual discrimination task. Supplementation with the Firm-5 species Lactobacillus apis, but not other non-Firm-5 bacterial species, enhances bees' memory. Untargeted metabolomics after L. apis supplementation show increased LPA (14:0) glycerophospholipid in the haemolymph. Oral administration of the LPA increases long-term memory significantly. Based on our findings and metagenomic/metabolomic analyses, we propose a molecular pathway for this gut-brain interaction. Our results provide insights into proximate and ultimate causes of cognitive differences in natural bumblebee populations.

Harmonic radar tracking reveals that honeybee drones navigate between multiple aerial leks.

Male honeybees (drones) are thought to congregate in large numbers in particular "drone congregation areas" to mate. We used harmonic radar to record the flight paths of individual drones and found that drones favored certain locations within the landscape which were stable over two years. Drones often visit multiple potential lekking sites within a single flight and take shared flight paths between them. Flights between such sites are relatively straight and begin as early as the drone's second flight, indicating familiarity with the sites acquired during initial learning flights. Arriving at congregation areas, drones display convoluted, looping flight patterns. We found a correlation between a drone's distance from the center of each area and its acceleration toward the center, a signature of collective behavior leading to congregation in these areas. Our study reveals the behavior of individual drones as they navigate between and within multiple aerial leks.

Animal Cognition: The Self-Image of a Bumblebee.

Knowing one's body dimensions is a core aspect of individual experience and self-awareness. A recent study illustrates how bees take into account their own body size both in preparation for and while traversing small gaps.

Different effects of reward value and saliency during bumblebee visual search for multiple rewarding targets.

Several animals, including bees, use visual search to distinguish targets of interest and ignore distractors. While bee flower choice is well studied, we know relatively little about how they choose between multiple rewarding flowers in complex floral environments. Two factors that could influence bee visual search for multiple flowers are the saliency (colour contrast against the background) and the reward value of flowers. We here investigated how these two different factors contribute to bee visual search. We trained bees to independently recognize two rewarding flower types that, in different experiments, differed in either saliency, reward value or both. We then measured their choices and attention to these flowers in the presence of distractors in a test without reinforcement. We found that bees preferred more salient or higher rewarding flowers and ignored distractors. When the high-reward flowers were less salient than the low-reward flowers, bees were nonetheless equally likely to choose high-reward flowers, for the reward and saliency values we used. Bees were also more likely to attend to these high-reward flowers, spending higher inspection times around them and exhibiting faster search times when choosing them. When flowers differed in reward, we also found an effect of the training order with low-reward targets being more likely to be chosen if they had been encountered during the more immediate training session prior to the test. Our results parallel recent findings from humans demonstrating that reward value can attract attention even when targets are less salient and irrelevant to the current task.