An 'instinct for learning': the learning flights and walks of bees, wasps and ants from the 1850s to now.

The learning flights and walks of bees, wasps and ants are precisely coordinated movements that enable insects to memorise the visual surroundings of their nest or other significant places such as foraging sites. These movements occur on the first few occasions that an insect leaves its nest. They are of special interest because their discovery in the middle of the 19th century provided perhaps the first evidence that insects can learn and are not solely governed by instinct. Here, we recount the history of research on learning flights from their discovery to the present day. The first studies were conducted by skilled naturalists and then, over the following 50 years, by neuroethologists examining the insects' learning behaviour in the context of experiments on insect navigation and its underlying neural mechanisms. The most important property of these movements is that insects repeatedly fixate their nest and look in other favoured directions, either in a preferred compass direction, such as North, or towards preferred objects close to the nest. Nest facing is accomplished through path integration. Memories of views along a favoured direction can later guide an insect's return to its nest. In some ant species, the favoured direction is adjusted to future foraging needs. These memories can then guide both the outward and homeward legs of a foraging trip. Current studies of central areas of the insect brain indicate what regions implement the behavioural manoeuvres underlying learning flights and the resulting visual memories.

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.

Wood ants learn the magnetic direction of a route but express uncertainty because of competing directional cues.

Wood ants were trained indoors to follow a magnetically specified route that went from the centre of an arena to a drop of sucrose at the edge. The arena, placed in a white cylinder, was in the centre of a 3D coil system generating an inclined Earth-strength magnetic field in any horizontal direction. The specified direction was rotated between each trial. The ants' knowledge of the route was tested in trials without food. Tests given early in the day, before any training, show that ants remember the magnetic route direction overnight. During the first 2 s of a test, ants mostly faced in the specified direction, but thereafter were often misdirected, with a tendency to face briefly in the opposite direction. Uncertainty about the correct path to take may stem in part from competing directional cues linked to the room. In addition to facing along the route, there is evidence that ants develop magnetically directed home and food vectors dependent upon path integration. A second experiment asked whether ants can use magnetic information contextually. In contrast to honeybees given a similar task, ants failed this test. Overall, we conclude that magnetic directional cues can be sufficient for route learning.

The routes of one-eyed ants suggest a revised model of normal route following.

The prevailing account of visually controlled routes is that an ant learns views as it follows a route, while guided by other path-setting mechanisms. Once a set of route views is memorised, the insect follows the route by turning and moving forwards when the view on the retina matches a stored view. We engineered a situation in which this account cannot suffice in order to discover whether there may be additional components to the performance of routes. One-eyed wood ants were trained to navigate a short route in the laboratory, guided by a single black, vertical bar placed in the blinded visual field. Ants thus had to turn away from the route to see the bar. They often turned to look at or beyond the bar and then turned to face in the direction of the goal. Tests in which the bar was shifted to be more peripheral or more frontal than in training produced a corresponding directional change in the ants' paths, demonstrating that they were guided by the bar. Examination of the endpoints of turns towards and away from the bar indicate that ants use the bar for guidance by learning how large a turn-back is needed to face the goal. We suggest that the ants' zigzag paths are, in part, controlled by turns of a learnt amplitude and that these turns are an integral component of visually guided route following.

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.

Path integration: how details of the honeybee waggle dance and the foraging strategies of desert ants might help in understanding its mechanisms.

Path integration is a navigational strategy that gives an animal an estimate of its position relative to some starting point. For many decades, ingenious and probing behavioural experiments have been the only window onto the operation of path integration in arthropods. New methods have now made it possible to visualise the activity of neural circuits in Drosophila while they fly or walk in virtual reality. Studies of this kind, as well as electrophysiological recordings from single neurons in the brains of other insects, are revealing details of the neural mechanisms that control an insect's direction of travel and other aspects of path integration. The aim here is first to review the major features of path integration in foraging desert ants and honeybees, the current champion path integrators of the insect world, and second consider how the elaborate behaviour of these insects might be accommodated within the framework of the newly understood neural circuits. The discussion focuses particularly on the ability of ants and honeybees to use a celestial compass to give direction in Earth-based coordinates, and of honeybees to use a landscape panorama to provide directional guidance for path integration. The possibility is raised that well-ordered behaviour might in some cases substitute for complex circuitry.

Insect learning flights and walks.

Knowledge of where things are in one's habitual surroundings cannot be encoded genetically and must be acquired in those surroundings. Many ants, bees and wasps forage from a home base and before doing so learn where resources are to be found and how to return with them to their nest. A significant component of this navigational learning seems to be the acquisition of panoramic views that insects record close to their nests and resource sites and along the paths between these places. Behavioural evidence indicates that these views are retinotopic, meaning, for instance, that an insect knows that it faces along a familiar route, if the image on its retina matches a view that it had previously recorded, when facing in that direction during route learning.

How does the insect central complex use mushroom body output for steering?

Research on central brain areas in Drosophila and other insects is revealing the highly conserved neural circuitries in the central complex that are responsible for course control using visual, ideothetic and compass cues [1,2], and in the mushroom bodies that hold long-term visual and olfactory memories [3,4]. Interactions between these areas are likely to be particularly important for navigation in which long-term memories determine an insect's course. Many ants, for example, use long-term visual memories for guidance along routes between their nest and food sites. But the interactions remain a puzzle: both because there are no known direct connections between mushroom body and central complex, and because the output from the mushroom body, where the route memories are probably stored [5], may simply signal whether a sensory input is attractive or aversive [4]. Extrapolating from a recent behavioural finding [6], we propose one way that the long-term memories in the mushroom body may be transformed into central complex steering commands. This answer, if correct, may reconcile two apparently conflicting ways of thinking about route following - suggesting how steering along a route can use a feedback controller based on a few prominent features [7], while the route memories themselves are holistic memories of the entire panorama [5]. It also suggests how visual navigation is related to (and possibly evolved from) visual targeting and olfactory-based guidance.

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.

Path Integration: Combining Optic Flow with Compass Orientation.

The discovery of translational optic flow detectors in the central complex of a bee has inspired a new model of path integration.

Insect Navigation: What Backward Walking Reveals about the Control of Movement.

Ants often walk backwards to drag large prey to their nest. New experiments show how they can use information from retinotopically encoded views to follow visual routes even while moving backwards. The mechanisms enabling ants to decouple body orientation and the control of travel direction are likely to be shared with other, flying, insects.

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.

On the Encoding of Panoramic Visual Scenes in Navigating Wood Ants.

A natural visual panorama is a complex stimulus formed of many component shapes. It gives an animal a sense of place and supplies guiding signals for controlling the animal's direction of travel [1]. Insects with their economical neural processing [2] are good subjects for analyzing the encoding and memory of such scenes [3-5]. Honeybees [6] and ants [7, 8] foraging from their nest can follow habitual routes guided only by visual cues within a natural panorama. Here, we analyze the headings that ants adopt when a familiar panorama composed of two or three shapes is manipulated by removing a shape or by replacing training shapes with unfamiliar ones. We show that (1) ants recognize a component shape not only through its particular visual features, but also by its spatial relation to other shapes in the scene, and that (2) each segmented shape [9] contributes its own directional signal to generating the ant's chosen heading. We found earlier that ants trained to a feeder placed to one side of a single shape [10] and tested with shapes of different widths learn the retinal position of the training shape's center of mass (CoM) [11, 12] when heading toward the feeder. They then guide themselves by placing the shape's CoM in the remembered retinal position [10]. This use of CoM in a one-shape panorama combined with the results here suggests that the ants' memory of a multi-shape panorama comprises the retinal positions of the horizontal CoMs of each major component shape within the scene, bolstered by local descriptors of that shape.

Insect Orientation: The Travails of Going Straight.

A study of dung beetles rolling dung balls to safety reveals unexpected facets of the beetle's acquisition and use of celestial information for keeping to a straight path.

When navigating wood ants use the centre of mass of a shape to extract directional information from a panoramic skyline.

Bees and ants can control their direction of travel within a familiar landscape using the information available in the surrounding visual scene. To learn more about the visual cues that contribute to this directional control, we have examined how wood ants obtain direction from a single shape that is presented in an otherwise uniform panorama. Earlier experiments revealed that when an ant's goal is aligned with a point within a prominent shape, the ant is guided by a global property of the shape: it learns the relative areas of the shape that lie to its left and right when facing the goal and sets its path by keeping the proportions at the memorised value. This strategy cannot be applied when the direction of the goal lies outside the shape. To see whether a different global feature of the shape might guide ants under these conditions, we trained ants to follow a direction to a point outside a single shape and then analysed their direction of travel when they were presented with different shapes. The tests indicate that ants learn the retinal position of the centre of mass of the training shape when facing the goal and can then guide themselves by placing the centre of mass of training and test shapes in this learnt position.

Insect Navigation: How Do Wasps Get Home?

Bees and wasps are famous for many things, including elaborate flights to learn where their nest is. A new study provides precise, three-dimensional details of a wasp's head and body movements during such flights and reconstructs what the wasp sees.

Route-segment odometry and its interactions with global path-integration.

Insects such as desert ants and honeybees use visual memories to travel along familiar routes between their nest and a food-site. We trained Cataglyphis fortis foragers along a two-segment route to investigate whether they encode the lengths of route segments over which visual cues remain approximately constant. Our results support earlier studies suggesting that such route-segment odometry exists, and allows an individual to stop using a visual route memory at an appropriate point, even in the absence of any change in the visual surroundings. But we find that the behavioural effects of route-segment odometry are often complicated by interactions with guidance from the global path-integration system. If route-segment odometry and path-integration agree, they act together to produce a precise signal for search. If the endpoint of route-segment odometry arrives first, it does not trigger search but its effect can persist and cause guidance by path-integration to end early. Conversely, if ants start with their path-integration state at zero, they follow a route memory for no more than 3 m, irrespective of the route-segment length. A possible explanation for these results is that if one guidance system is made to overshoot its endpoint, it can cause the other to be cut short.

Insect navigation: do honeybees learn to follow highways?

Radar studies of a honeybee's flights when it first leaves its nest suggest the features of the surrounding landscape that it learns guide future foraging trips.

Head movements and the optic flow generated during the learning flights of bumblebees.

Insects inform themselves about the 3D structure of their surroundings through motion parallax. During flight, they often simplify this task by minimising rotational image movement. Coordinated head and body movements generate rapid shifts of gaze separated by periods of almost zero rotational movement, during which the distance of objects from the insect can be estimated through pure translational optic flow. This saccadic strategy is less appropriate for assessing the distance between objects. Bees and wasps face this problem when learning the position of their nest-hole relative to objects close to it. They acquire the necessary information during specialised flights performed on leaving the nest. Here, we show that the bumblebee's saccadic strategy differs from other reported cases. In the fixations between saccades, a bumblebee's head continues to turn slowly, generating rotational flow. At specific points in learning flights these imperfect fixations generate a form of 'pivoting parallax', which is centred on the nest and enhances the visibility of features near the nest. Bumblebees may thus utilize an alternative form of motion parallax to that delivered by the standard 'saccade and fixate' strategy in which residual rotational flow plays a role in assessing the distances of objects from a focal point of interest.