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.

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.

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 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.

Small and Large Bumblebees Invest Differently when Learning about Flowers.

Honeybees and bumblebees 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.

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 while they fly or walk in virtual reality.

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.

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.

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.

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.

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].

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.

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.

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.

Scene perception and the visual control of travel direction in navigating wood ants.

This review reflects a few of Mike Land's many and varied contributions to visual science. In it, we show for wood ants, as Mike has done for a variety of animals, including readers of this piece, what can be learnt from a detailed analysis of an animal's visually guided eye, head or body movements. In the case of wood ants, close examination of their body movements, as they follow visually guided routes, is starting to reveal how they perceive and respond to their visual world and negotiate a path within it.

Phase-dependent visual control of the zigzag paths of navigating wood ants.

Animals sometimes take sinuous paths to a goal. Insects, tracking an odor trail on the ground [1-3] or moving up an odor plume in the air [4, 5], generally follow zigzag paths. Some insects [6-8] take a zigzag approach to visual targets, perhaps to obtain parallax information.

Spatial memory in insect navigation.

A wide variety of insects use spatial memories in behaviours like holding a position in air or flowing water, in returning to a place of safety, and in foraging. The Hymenoptera, in particular, have evolved life-histories requiring reliable spatial memories to support the task of provisioning their young. Behavioural experiments, primarily on social bees and ants, reveal the mechanisms by which these memories are employed for guidance to spatial goals and suggest how the memories, and the processing streams that use them, may be organized.

Visual scene perception in navigating wood ants.

Ants, like honeybees, can set their travel direction along foraging routes using just the surrounding visual panorama. This ability gives us a way to explore how visual scenes are perceived. By training wood ants to follow a path in an artificial scene and then examining their path within transformed scenes, we identify several perceptual operations that contribute to the ants' choice of direction.

Coordinating compass-based and nest-based flight directions during bumblebee learning and return flights.

Bumblebees tend to face their nest over a limited range of compass directions when learning the nest's location on departure and finding it on their approach after foraging. They thus obtain similar views of the nest and its surroundings on their learning and return flights. How do bees coordinate their flights relative to nest-based and compass-based reference frames to get such similar views? We show, first, that learning and return flights contain straight segments that are directed along particular compass bearings, which are independent of the orientation of a bee's body.