Learning modifies attention during bumblebee visual search.

Abstract: The role of visual search during bee foraging is relatively understudied compared to the choices made by bees. As bees learn about rewards, we predicted that visual search would be modified to prioritise rewarding flowers. To test this, we ran an experiment testing how bee search differs in the initial and later part of training as they learn about flowers with either higher- or lower-quality rewards. We then ran an experiment to see how this prior training with reward influences their search on a subsequent task with different flowers. We used the time spent inspecting flowers as a measure of attention and found that learning increased attention to rewards and away from unrewarding flowers. Higher quality rewards led to decreased attention to non-flower regions, but lower quality rewards did not. Prior experience of lower rewards also led to more attention to higher rewards compared to unrewarding flowers and non-flower regions. Our results suggest that flowers would elicit differences in bee search behaviour depending on the sugar content of their nectar. They also demonstrate the utility of studying visual search and have important implications for understanding the pollination ecology of flowers with different qualities of reward. Significance statement: Studies investigating how foraging bees learn about reward typically focus on the choices made by the bees. How bees deploy attention and visual search during foraging is less well studied. We analysed flight videos to characterise visual search as bees learn which flowers are rewarding. We found that learning increases the focus of bees on flower regions. We also found that the quality of the reward a flower offers influences how much bees search in non-flower areas. This means that a flower with lower reward attracts less focussed foraging compared to one with a higher reward. Since flowers do differ in floral reward, this has important implications for how focussed pollinators will be on different flowers. Our approach of looking at search behaviour and attention thus advances our understanding of the cognitive ecology of pollination. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-024-03432-z.

How bumblebees coordinate path integration and body orientation at the start of their first learning flight.

The start of a bumblebee's first learning flight from its nest provides an opportunity to examine the bee's learning behaviour during its initial view of the nest's unfamiliar surroundings. Like many other hymenopterans, bumblebees store views of their nest surroundings while facing their nest. We found that a bumblebee's first fixation of the nest is a coordinated manoeuvre in which the insect faces the nest with its body oriented towards a particular visual feature within its surroundings. This conjunction of nest fixation and body orientation is preceded and reached by means of a translational scan during which the bee flies perpendicularly to its preferred body orientation. The utility of the coordinated manoeuvre is apparent during the bees' first return flight after foraging. Bees then adopt a similar preferred body orientation when close to the nest. How does a bee, unacquainted with its surroundings, know when it is facing its nest? A likely answer is through path integration, which gives bees continuously updated information about the current direction of their nest. Path integration also gives bees the possibility to fixate the nest when their body points in a desired direction. The three components of this coordinated manoeuvre are discussed in relation to current understanding of the central complex in the insect brain, noting that nest fixation is egocentric, whereas the preferred body orientation and flight direction that the bee adopts within the visual surroundings of the nest are geocentric.

Onset of morning activity in bumblebee foragers under natural low light conditions.

Foraging on flowers in low light at dusk and dawn comes at an additional cost for insect pollinators with diurnal vision. Nevertheless, some species are known to be frequently active at these times. To explore how early and under which light levels colonies of bumblebees, Bombus terrestris, initiate their foraging activity, we tracked foragers of different body sizes using RFID over 5 consecutive days during warm periods of the flowering season. Bees that left the colony at lower light levels and earlier in the day were larger in size. This result extends the evidence for alloethism in bumblebees and shows that foragers differ in their task specialization depending on body size. By leaving the colony earlier to find and exploit flowers in low light, larger-sized foragers are aided by their more sensitive eyes and can effectively increase their contributions to the colony's food influx. The decision to leave the colony early seems to be further facilitated by knowledge about profitable food resources in specific locations. We observed that experience accrued over many foraging flights determined whether a bee started foraging under lower light levels and earlier in the morning. Larger-sized bees were not more experienced than smaller-sized bees, confirming earlier observations of wide size ranges among active foragers. Overall, we found that most foragers left at higher light levels when they could see well and fly faster. Nevertheless, a small proportion of foragers left the colony shortly after the onset of dawn when light levels were below 10 lux. Our observations suggest that bumblebee colonies have the potential to balance the benefits of deploying large-sized or experienced foragers during dawn against the risks and costs of foraging under low light by regulating the onset of their activity at different stages of the colony's life cycle and in changing environmental conditions.

Small and Large Bumblebees Invest Differently when Learning about Flowers.

Honeybees1 and bumblebees2 perform learning flights when leaving a newly discovered flower. During these flights, bees spend a portion of the time turning back to face the flower when they can memorize views of the flower and its surroundings. In honeybees, learning flights become longer when the reward offered by a flower is increased.3 We show here that bumblebees behave in a similar way, and we add that bumblebees face an artificial flower more when the concentration of the sucrose solution that the flower provides is higher. The surprising finding is that a bee's size determines what a bumblebee regards as a "low" or "high" concentration and so affects its learning behavior. The larger bees in a sample of foragers only enhance their flower facing when the sucrose concentration is in the upper range of the flowers that are naturally available to bees.4 In contrast, smaller bees invest the same effort in facing flowers whether the concentration is high or low, but their effort is less than that of larger bees. The way in which different-sized bees distribute their effort when learning about flowers parallels the foraging behavior of a colony. Large bumblebees5,6 are able to carry larger loads and explore further from the nest than smaller ones.7 Small ones with a smaller flight range and carrying capacity cannot afford to be as selective and so accept a wider range of flowers. VIDEO ABSTRACT.

Inhibitory control and memory in the search process for a modified problem in grey squirrels, Sciurus carolinensis.

Inhibiting learned behaviours when they become unproductive and searching for an alternative solution to solve a familiar but different problem are two indicators of flexibility in problem solving. A wide range of animals show these tendencies spontaneously, but what kind of search process is at play behind their problem-solving success? Here, we investigated how Eastern grey squirrels, Sciurus carolinensis, solved a modified mechanical problem that required them to abandon their preferred and learned solution and search for alternative solutions to retrieve out-of-reach food rewards. Squirrels could solve the problem by engaging in either an exhaustive search (i.e., using trial-and-error to access the reward) or a 'backup' solution search (i.e., recalling a previously successful but non-preferred solution). We found that all squirrels successfully solved the modified problem on their first trial and showed solving durations comparable to their last experience of using their preferred solution. Their success and high efficiency could be explained by their high level of inhibitory control as the squirrels did not persistently emit the learned and preferred, but now ineffective, pushing behaviour. Although the squirrels had minimal experience in using the alternative (non-preferred) successful solution, they used it directly or after one or two failed attempts to achieve success. Thus, the squirrels were using the 'backup' solution search process. Such a process is likely a form of generalisation which involves retrieving related information of an experienced problem and applying previous successful experience during problem solving. Overall, our results provide information regarding the search process underlying the flexibility observable in problem-solving success.

Variations on a theme: bumblebee learning flights from the nest and from flowers.

On leaving a significant place to which they will return, bees and wasps perform learning flights to acquire visual information to guide them back. The flights are set in different contexts, such as from their nest or a flower, which are functionally and visually different. The permanent and inconspicuous nest hole of a bumblebee worker is locatable primarily through nearby visual features, whereas a more transient flower advertises itself by its colour and shape. We compared the learning flights of bumblebees leaving their nest or a flower in an experimental situation in which the nest hole, flower and their surroundings were visually similar. Consequently, differences in learning flights could be attributed to the bee's internal state when leaving the nest or flower rather than to the visual scene. Flights at the flower were a quarter as long as those at the nest and more focused on the flower than its surroundings. Flights at the nest covered a larger area with the bees surveying a wider range of directions. For the initial third of the learning flight, bees kept within about 5 cm of the flower and nest hole, and tended to face and fixate the nest, flower and nearby visual features. The pattern of these fixations varied between nest and flower, and these differences were reflected in the bees' return flights to the nest and flower. Together, these findings suggest that learning flights are tuned to the bees' inherent expectations of the visual and functional properties of nests and flowers.

How to stay perfect: the role of memory and behavioural traits in an experienced problem and a similar problem.

When animals encounter a task they have solved previously, or the same problem appears in a different apparatus, how does memory, alongside behavioural traits such as persistence, selectivity and flexibility, enhance problem-solving efficiency? We examined this question by first presenting grey squirrels with a puzzle 22 months after their last experience of it (the recall task). Squirrels were then given the same problem presented in a physically different apparatus (the generalisation task) to test whether they would apply the previously learnt tactics to solve the same problem but in a different apparatus. The mean latency to success in the first trial of the recall task was significantly different from the first exposure but not different from the last exposure of the original task, showing retention of the task. A neophobia test in the generalisation task suggested squirrels perceived the different apparatus as a different problem, but they quickly came to apply the same effective tactics as before to solve the task. Greater selectivity (the proportion of effective behaviours) and flexibility (the rate of switching between tactics) both enhanced efficiency in the recall task, but only selectivity enhanced efficiency in the generalisation task. These results support the interaction between memory and behavioural traits in problem-solving, in particular memory of task-specific tactics that could enhance efficiency. Squirrels remembered and emitted task-effective tactics more than ineffective tactics. As a result, they consistently changed from ineffective to effective behaviours after failed attempts at problem-solving.

Male bumblebees perform learning flights on leaving a flower but not when leaving their nest.

Female bees and wasps demonstrate, through their performance of elaborate learning flights, when and where they memorise features of a significant site. An important feature of these flights is that the insects look back to fixate the site that they are leaving. Females, which forage for nectar and pollen and return with it to the nest, execute learning flights on their initial departure from both their nest and newly discovered flowers. To our knowledge, these flights have so far only been studied in females. Here, we describe and analyse putative learning flights observed in male bumblebees Bombus terrestris L. Once male bumblebees are mature, they leave their nest for good and fend for themselves. We show that, unlike female foragers, males always fly directly away from their nest, without looking back, in keeping with their indifference to their natal nest. In contrast, after males have drunk from artificial flowers, their flights on first leaving the flowers resemble the learning flights of females, particularly in their fixation of the flowers. These differences in the occurrence of female and male learning flights seem to match the diverse needs of the two sexes to learn about disparate, ecologically relevant places in their surroundings.