Evidence for socially influenced and potentially actively coordinated cooperation by bumblebees.

Cooperation is common in animals, yet the specific mechanisms driving collaborative behaviour in different species remain unclear. We investigated the proximate mechanisms underlying the cooperative behaviour of bumblebees in two different tasks, where bees had to simultaneously push a block in an arena or a door at the end of a tunnel for access to reward. In both tasks, when their partner's entry into the arena/tunnel was delayed, bees took longer to first push the block/door compared with control bees that learned to push alone. In the tunnel task, just before gaining access to reward, bees were more likely to face towards their partner than expected by chance or compared with controls. These results show that bumblebees' cooperative behaviour is not simply a by-product of individual efforts but is socially influenced. We discuss how bees' turning behaviours, e.g. turning around before first reaching the door when their partner was delayed and turning back towards the door in response to seeing their partner heading towards the door, suggest the potential for active coordination. However, because these behaviours could also be interpreted as combined responses to social and secondary reinforcement cues, future studies are needed to help clarify whether bumblebees truly use active coordination.

The role of cognition in nesting.

For many animals, nests are essential for reproductive success. Nesting individuals need to carry out a range of potentially challenging tasks, from selecting an appropriate site and choosing suitable materials to constructing the nest and defending it against competitors, parasites and predators. Given the high fitness stakes involved, and the diverse impacts both the abiotic and social environment can have on nesting success, we might expect cognition to facilitate nesting efforts. This should be especially true under variable environmental conditions, including those changing due to anthropogenic impacts. Here, we review, across a wide range of taxa, evidence linking cognition to nesting behaviours, including selection of nesting sites and materials, nest construction, and nest defence. We also discuss how different cognitive abilities may increase an individual's nesting success. Finally, we highlight how combining experimental and comparative research can uncover the links between cognitive abilities, nesting behaviours and the evolutionary pathways that may have led to the associations between them. In so doing, the review highlights current knowledge gaps and provides suggestions for future research. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Field-realistic acute exposure to glyphosate-based herbicide impairs fine-color discrimination in bumblebees.

Pollinator decline is a grave challenge worldwide. One of the main culprits for this decline is the widespread use of, and pollinators' chronic exposure to, agrochemicals. Here, we examined the effect of a field-realistic dose of the world's most commonly used pesticide, glyphosate-based herbicide (GBH), on bumblebee cognition. We experimentally tested bumblebee (Bombus terrestris) color and scent discrimination using acute GBH exposure, approximating a field-realistic dose from a day's foraging in a patch recently sprayed with GBH. In a 10-color discrimination experiment with five learning bouts, GBH treated bumblebees' learning rate fell to zero by third learning bout, whereas the control bees increased their performance in the last two bouts. In the memory test, the GBH treated bumblebees performed to near chance level, indicating that they had lost everything they had learned during the learning bouts, while the control bees were performing close to the level in their last learning bout. However, GBH did not affect bees' learning in a 2-color or 10-odor discrimination experiment, which suggests that the impact is limited to fine color learning and does not necessarily generalize to less specific tasks or other modalities. These results indicate that the widely used pesticide damages bumblebees' fine-color discrimination, which is essential to the pollinator's individual success and to colony fitness in complex foraging environments. Hence, our study suggests that acute sublethal exposure to GBH poses a greater threat to pollination-based ecosystem services than previously thought, and that tests for learning and memory should be integrated into pesticide risk assessment.

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.

Vocal accommodation in penguins (Spheniscus demersus) as a result of social environment.

The ability to vary the characteristics of one's voice is a critical feature of human communication. Understanding whether and how animals change their calls will provide insights into the evolution of language. We asked to what extent the vocalizations of penguins, a phylogenetically distant species from those capable of explicit vocal learning, are flexible and responsive to their social environment. Using a principal components (PCs) analysis, we reduced 14 vocal parameters of penguin's contact calls to four PCs, each comprising highly correlated parameters and which can be categorized as fundamental frequency, formant frequency, frequency modulation, and amplitude modulation rate and duration. We compared how these differed between individuals with varying degrees of social interactions: same-colony versus different-colony, same colony over 3 years and partners versus non-partners. Our analyses indicate that the more penguins experience each other's calls, the more similar their calls become over time, that vocal convergence requires a long time and relative stability in colony membership, and that partners' unique social bond may affect vocal convergence differently than non-partners. Our results suggest that this implicit form of vocal plasticity is perhaps more widespread across the animal kingdom than previously thought and may be a fundamental capacity of vertebrate vocalization.

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.

Cross-modal individual recognition in the African penguin and the effect of partnership.

An animal's ability to recognize another individual by matching their image to their voice suggests they form internal representations of other individuals. To what extent this ability, termed cross-modal individual recognition, extends to birds other than corvids is unknown. Here, we used an expectancy violation paradigm to determine whether a monogamous territorial seabird (Spheniscus demersus) can cross-modally recognize familiar conspecifics (partners or colony-mates). After pairs of penguins spent time together in an isolated area, one of the penguins was released from the area leaving the focal penguin alone. Subsequently, we played contact calls of the released penguin (congruent condition) or a different penguin (incongruent condition). After being paired with a colony-mate, focal penguins' response latency to the auditory stimulus was faster in the incongruent compared to congruent condition, indicating the mismatch violated their expectations. This behavioural pattern was not observed in focal penguins after being paired with their partner. We discuss these different results in the light of penguins' natural behaviour and the evolution of social communication strategies. Our results suggest that cross-modal individual recognition extends to penguins and reveals, in contrast with previously thought, that social communication between members of this endangered species can also use visual cues.

Non-numerical strategies used by bees to solve numerical cognition tasks.

We examined how bees solve a visual discrimination task with stimuli commonly used in numerical cognition studies. Bees performed well on the task, but additional tests showed that they had learned continuous (non-numerical) cues. A network model using biologically plausible visual feature filtering and a simple associative rule was capable of learning the task using only continuous cues inherent in the training stimuli, with no numerical processing. This model was also able to reproduce behaviours that have been considered in other studies indicative of numerical cognition. Our results support the idea that a sense of magnitude may be more primitive and basic than a sense of number. Our findings highlight how problematic inadvertent continuous cues can be for studies of numerical cognition. This remains a deep issue within the field that requires increased vigilance and cleverness from the experimenter. We suggest ways of better assessing numerical cognition in non-speaking animals, including assessing the use of all alternative cues in one test, using cross-modal cues, analysing behavioural responses to detect underlying strategies, and finding the neural substrate.

Foraging Bumblebees Selectively Attend to Other Types of Bees Based on Their Reward-Predictive Value.

Using social information can be an efficient strategy for learning in a new environment while reducing the risks associated with trial-and-error learning. Whereas social information from conspecifics has long been assumed to be preferentially attended by animals, heterospecifics can also provide relevant information. Because different species may vary in their informative value, using heterospecific social information indiscriminately can be ineffective and even detrimental. Here, we evaluated how selective use of social information might arise at a proximate level in bumblebees (Bombus terrestris) as a result of experience with demonstrators differing in their visual appearance and in their informative value as reward predictors. Bumblebees were first trained to discriminate rewarding from unrewarding flowers based on which type of "heterospecific" (one of two differently painted model bees) was next to each flower. Subsequently, these bumblebees were exposed to a novel foraging context with two live painted bees. In this novel context, observer bumblebees showed significantly more social information-seeking behavior towards the type of bees that had predicted reward during training. Bumblebees were not attracted by paint-marked small wooden balls (moved via magnets) or paint-marked non-pollinating heterospecifics (woodlice; Porcellio laevis) in the novel context, indicating that bees did not simply respond to conditioned color cues nor to irrelevant social cues, but rather had a "search image" of what previously constituted a valuable, versus invaluable, information provider. The behavior of our bumblebees suggests that their use of social information is governed by learning, is selective, and extends beyond conspecifics.

Bumblebees Learn a Relational Rule but Switch to a Win-Stay/Lose-Switch Heuristic After Extensive Training.

Mapping animal performance in a behavioral task to underlying cognitive mechanisms and strategies is rarely straightforward, since a task may be solvable in more than one manner. Here, we show that bumblebees perform well on a concept-based visual discrimination task but spontaneously switch from a concept-based solution to a simpler heuristic with extended training, all while continually increasing performance. Bumblebees were trained in an arena to find rewards on displays with shapes of different sizes where they could not use low-level visual cues. One group of bees was rewarded at displays with larger shapes and another group at displays with smaller shapes. Analysis of total choices shows bees increased their performance over 30 bouts to above chance. However, analyses of first and sequential choices suggest that after approximately 20 bouts, bumblebees changed to a win-stay/lose-switch strategy. Comparing bees' behavior to a probabilistic model based on a win-stay/lose-switch strategy further supports the idea that bees changed strategies with extensive training. Analyses of unrewarded tests indicate that bumblebees learned and retained the concept of relative size even after they had already switched to a win-stay, lost-shift strategy. We propose that the reason for this strategy switching may be due to cognitive flexibility and efficiency.

Bumble bees display cross-modal object recognition between visual and tactile senses.

Many animals can associate object shapes with incentives. However, such behavior is possible without storing images of shapes in memory that are accessible to more than one sensory modality. One way to explore whether there are modality-independent internal representations of object shapes is to investigate cross-modal recognition-experiencing an object in one sensory modality and later recognizing it in another. We show that bumble bees trained to discriminate two differently shaped objects (cubes and spheres) using only touch (in darkness) or vision (in light, but barred from touching the objects) could subsequently discriminate those same objects using only the other sensory information. Our experiments demonstrate that bumble bees possess the ability to integrate sensory information in a way that requires modality-independent internal representations.

Bumblebees show cognitive flexibility by improving on an observed complex behavior.

We explored bees' behavioral flexibility in a task that required transporting a small ball to a defined location to gain a reward. Bees were pretrained to know the correct location of the ball. Subsequently, to obtain a reward, bees had to move a displaced ball to the defined location. Bees that observed demonstration of the technique from a live or model demonstrator learned the task more efficiently than did bees observing a "ghost" demonstration (ball moved via magnet) or without demonstration. Instead of copying demonstrators moving balls over long distances, observers solved the task more efficiently, using the ball positioned closest to the target, even if it was of a different color than the one previously observed. Such unprecedented cognitive flexibility hints that entirely novel behaviors could emerge relatively swiftly in species whose lifestyle demands advanced learning abilities, should relevant ecological pressures arise.

Unexpected rewards induce dopamine-dependent positive emotion-like state changes in bumblebees.

Whether invertebrates exhibit positive emotion-like states and what mechanisms underlie such states remain poorly understood. We demonstrate that bumblebees exhibit dopamine-dependent positive emotion-like states across behavioral contexts. After training with one rewarding and one unrewarding cue, bees that received pretest sucrose responded in a positive manner toward ambiguous cues. In a second experiment, pretest consumption of sucrose solution resulted in a shorter time to reinitiate foraging after a simulated predator attack. These behavioral changes were abolished with topical application of the dopamine antagonist fluphenazine. Further experiments established that pretest sucrose does not simply cause bees to become more exploratory. Our findings present a new opportunity for understanding the fundamental neural elements of emotions and may alter the view of how emotion states affect decision-making in animals.