Learning Flights Research Articles

Cognitive abilities related to foraging behavior in Vespula vulgaris (Hymenoptera: Vespidae)

Vespula vulgaris is an invasive social wasp that has become established in many parts of the world. Plastic cognitive systems are expected to be advantageous for invasive species, given that they continuously face dynamic and unpredictable environments. We analyzed foraging behavior associated with undepleted and depleted resources. The wasps were trained to associate a certain location with food and we recorded their behavior after successive displacement of it. We also studied how long wasps continued to search for food that was no longer available and whether it was dependent on experience. We found that when wasps associated a certain location with food, they returned to the same site even though food was no longer available or had been displaced. Handling time remained constant, while relocation time and learning flights decreased with experience. With a food position change, learning flights increased and searching time varied with experience. When food was removed, hovering and landings were greatest in wasps that had the most experience with the resource, although extinction of the searching response was not dependent on experience. Our results illustrate the plasticity of wasp behavior in uncertain foraging contexts, which could have allowed the species to establish successfully in new habitats.

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.

Visual navigation: properties, acquisition and use of views.

Panoramic views offer information on heading direction and on location to visually navigating animals. This review covers the properties of panoramic views and the information they provide to navigating animals, irrespective of image representation. Heading direction can be retrieved by alignment matching between memorized and currently experienced views, and a gradient descent in image differences can lead back to the location at which a view was memorized (positional image matching). Central place foraging insects, such as ants, bees and wasps, conduct distinctly choreographed learning walks and learning flights upon first leaving their nest that are likely to be designed to systematically collect scene memories tagged with information provided by path integration on the direction of and the distance to the nest. Equally, traveling along routes, ants have been shown to engage in scanning movements, in particular when routes are unfamiliar, again suggesting a systematic process of acquiring and comparing views. The review discusses what we know and do not know about how view memories are represented in the brain of insects, how they are acquired and how they are subsequently used for traveling along routes and for pinpointing places.

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

SummaryMale 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.

The Critical Role of Head Movements for Spatial Representation During Bumblebees Learning Flight.

Bumblebees perform complex flight maneuvers around the barely visible entrance of their nest upon their first departures. During these flights bees learn visual information about the surroundings, possibly including its spatial layout. They rely on this information to return home. Depth information can be derived from the apparent motion of the scenery on the bees' retina. This motion is shaped by the animal's flight and orientation: Bees employ a saccadic flight and gaze strategy, where rapid turns of the head (saccades) alternate with flight segments of apparently constant gaze direction (intersaccades). When during intersaccades the gaze direction is kept relatively constant, the apparent motion contains information about the distance of the animal to environmental objects, and thus, in an egocentric reference frame. Alternatively, when the gaze direction rotates around a fixed point in space, the animal perceives the depth structure relative to this pivot point, i.e., in an allocentric reference frame. If the pivot point is at the nest-hole, the information is nest-centric. Here, we investigate in which reference frames bumblebees perceive depth information during their learning flights. By precisely tracking the head orientation, we found that half of the time, the head appears to pivot actively. However, only few of the corresponding pivot points are close to the nest entrance. Our results indicate that bumblebees perceive visual information in several reference frames when they learn about the surroundings of a behaviorally relevant location.

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.

The learning walks of ants (Hymenoptera: Formicidae)

When transitioning from in-nest duties to their foraging life outside the nest, ants perform a series of highly choreo-graphed learning walks around the nest entrance, before leaving to forage for the first time. These learning walks have been described in detail only for a few species of ants, but a pattern of similarities and differences is emerging that we review here with an emphasis on understanding the functional significance of this learning process for efficient homing in ants. We compare the organization of learning walks in ants with that of the learning flights in bees and wasps and provide a list of key research questions that would need to be tackled if we are to understand the role of learning walks in the acquisition of nest-location information, the evolution of this highly conserved learning process, and how it is controlled.Open access, licensed under CC BY 4.0. © 2019 The Author(s)DOI: 10.25849/myrmecol.news_029:093Pages: 93-110Volume: 29Year: 2019Journal: Myrmecol. News

An insect-inspired model for acquiring views for homing.

Wasps and bees perform learning flights when leaving their nest or food locations for the first time during which they acquire visual information that enables them to return successfully. Here we present and test a set of simple control rules underlying the execution of learning flights that closely mimic those performed by ground-nesting wasps. In the simplest model, we assume that the angle between flight direction and the nest direction as seen from the position of the insect is constant and only flips sign when pivoting direction around the nest is changed, resulting in a concatenation of piecewise defined logarithmic spirals. We then added characteristic properties of real learning flights, such as head saccades and the condition that the nest entrance within the visual field is kept nearly constant to describe the development of a learning flight in a head-centered frame of reference, assuming that the retinal position of the nest is known. We finally implemented a closed-loop simulation of learning flights based on a small set of visual control rules. The visual input for this model are rendered views generated from 3D reconstructions of natural wasp nesting sites, and the retinal nest position is controlled by means of simple template-based tracking. We show that naturalistic paths can be generated without knowledge of the absolute distance to the nest or of the flight speed. We demonstrate in addition that nest-tagged views recorded during such simulated learning flights are sufficient for a homing agent to pinpoint the goal, by identifying nest direction when encountering familiar views. We discuss how the information acquired during learning flights close to the nest can be integrated with long-range homing models.

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.

The role of spatial texture in visual control of bumblebee learning flights

When leaving the nest for the first time, bees and wasps perform elaborate learning flights, during which the location of the nest is memorised. These flights are characterised by a succession of arcs or loops of increasing radius centred around the nest, with an incremental increase in ground speed, which requires precise control of the flight manoeuvres by the insect. Here, we investigated the role of optic flow cues in the control of learning flights by manipulating spatial texture in the ventral and panoramic visual field. We measured height, lateral displacement relative to the nest and ground speed during learning flights in bumblebees when ventral and panoramic optic flow cues were present or minimised, or features of the ground texture varied in size. Our observations show that ventral optic flow cues were required for the smooth execution of learning flights. We also found that bumblebees adjusted their flight height in response to variations of the visual texture on the ground. However, the presence or absence of panoramic optic flow did not have a substantial effect on flight performance. Our findings suggest that bumblebees mainly rely on optic flow information from the ventral visual field to control their learning flights.

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 Wasps Acquire and Use Views for Homing

Nesting insects perform learning flights to establish a visual representation of the nest environment that allows them to subsequently return to the nest. It has remained unclear when insects learn what during these flights, what determines their overall structure, and, in particular, how what is learned is used to guide an insect's return. We analyzed learning flights in ground-nesting wasps (Sphecidae: Cerceris australis) using synchronized high-speed cameras to determine 3D head position and orientation. Wasps move along arcs centered on the nest entrance, whereby rapid changes in gaze assure that the nest is seen at lateral positions in the left or the right visual field. Between saccades, the wasps translate along arc segments around the nest while keeping gaze fixed. We reconstructed panoramic views along the paths of learning and homing wasps to test specific predictions about what wasps learn during their learning flights and how they use this information to guide their return. Our evidence suggests that wasps monitor changing views during learning flights and use the differences they experience relative to previously encountered views to decide when to begin a new arc. Upon encountering learned views, homing wasps move left or right, depending on the nest direction associated with that view, and in addition appear to be guided by features on the ground close to the nest. We test our predictions on how wasps use views for homing by simulating homing flights of a virtual wasp guided by views rendered in a 3D model of a natural wasp environment.

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.

Target Detection Is Enhanced by Polarization Vision in a Fiddler Crab

We are constantly surprised by the ability of relatively simple animals to perform precise visually guided movements within complex visual scenes, often using eyes with limited resolution. Exceptional examples include the capture of airborne prey by dragonflies, the learning flights of bees and wasps, and the tracking of conspecifics by crabs on intertidal mudflats. Most studies have focused on how animals do this using sensitivity to intensity or color. However, it is increasingly evident that a third ability, polarization vision, may contribute to such tasks. In many insects, polarization-sensitive photoreceptors are confined within an area of the eye known as the dorsal rim, which detects the polarized sky pattern specifically for navigation. However, some animals, including fiddler crabs, are sensitive to the polarization of light across the majority of their image-forming eyes, potentially allowing them to use polarization information to increase perceived contrast for general visual tasks. Investigations into the use of polarization image-parsing by animals have largely been confined to laboratory settings under artificial lighting. This approach can occasionally mislead if the lighting conditions are different from natural. This study presents the first behavioral evidence from the natural context for a function of polarization image parsing. Using experimental manipulations in wild populations of the fiddler crab Uca stenodactylus, we provide evidence that these animals use their polarization vision to enhance contrast in their visual environment, thereby increasing their ability to detect and respond to objects on the mudflat surface.

Effect of Magnetic Field on the Foraging Rhythm and Behavior of the Swarm-founding Paper Wasp Polybia paulista Ihering (hymenoptera: vespidae)

The geomagnetic field can be used by insects for navigation and orientation, through different magnetoreception mechanisms. Magnetic sensitivity is very well documented in honeybees, ants and termites, but few studies have examined this capability in social wasps. The present study analyzed the magnetic sensitivity of the paper wasp Polybia paulista . The wasps' behavior was analyzed in the normal geomagnetic field and in the presence of external magnetic fields generated by permanent magnets or by Helmholtz coils. The frequency of foraging flights was measured in both conditions, and also the behavior of the individuals on the nest surface was analyzed. The magnetic field from the permanent magnet produced an increase in the frequency of departing foraging flights, and also the wasps grouped together on the nest surface in front of the magnet. The electromagnetic field created by the Helmholtz coils also increased foraging flights, but individuals did not show grouping behavior. This Helmholtz electromagnetic field induced wasp workers to perform “learning flights”. These results show for the first time that Polybia paulista wasps are sensitive to magnetic fields, including it in the list of animal models to study magnetoreception and magnetic sensitivity.

Visual motion-sensitive neurons in the bumblebee brain convey information about landmarks during a navigational task.

Bees use visual memories to find the spatial location of previously learnt food sites. Characteristic learning flights help acquiring these memories at newly discovered foraging locations where landmarks—salient objects in the vicinity of the goal location—can play an important role in guiding the animal's homing behavior. Although behavioral experiments have shown that bees can use a variety of visual cues to distinguish objects as landmarks, the question of how landmark features are encoded by the visual system is still open. Recently, it could be shown that motion cues are sufficient to allow bees localizing their goal using landmarks that can hardly be discriminated from the background texture. Here, we tested the hypothesis that motion sensitive neurons in the bee's visual pathway provide information about such landmarks during a learning flight and might, thus, play a role for goal localization. We tracked learning flights of free-flying bumblebees (Bombus terrestris) in an arena with distinct visual landmarks, reconstructed the visual input during these flights, and replayed ego-perspective movies to tethered bumblebees while recording the activity of direction-selective wide-field neurons in their optic lobe. By comparing neuronal responses during a typical learning flight and targeted modifications of landmark properties in this movie we demonstrate that these objects are indeed represented in the bee's visual motion pathway. We find that object-induced responses vary little with object texture, which is in agreement with behavioral evidence. These neurons thus convey information about landmark properties that are useful for view-based homing.

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.

The ontogeny of bumblebee flight trajectories: from naïve explorers to experienced foragers.

Understanding strategies used by animals to explore their landscape is essential to predict how they exploit patchy resources, and consequently how they are likely to respond to changes in resource distribution. Social bees provide a good model for this and, whilst there are published descriptions of their behaviour on initial learning flights close to the colony, it is still unclear how bees find floral resources over hundreds of metres and how these flights become directed foraging trips. We investigated the spatial ecology of exploration by radar tracking bumblebees, and comparing the flight trajectories of bees with differing experience. The bees left the colony within a day or two of eclosion and flew in complex loops of ever-increasing size around the colony, exhibiting Lévy-flight characteristics constituting an optimal searching strategy. This mathematical pattern can be used to predict how animals exploring individually might exploit a patchy landscape. The bees’ groundspeed, maximum displacement from the nest and total distance travelled on a trip increased significantly with experience. More experienced bees flew direct paths, predominantly flying upwind on their outward trips although forage was available in all directions. The flights differed from those of naïve honeybees: they occurred at an earlier age, showed more complex looping, and resulted in earlier returns of pollen to the colony. In summary bumblebees learn to find home and food rapidly, though phases of orientation, learning and searching were not easily separable, suggesting some multi-tasking.

Bumblebee calligraphy: the design and control of flight motifs in the learning and return flights ofBombus terrestris

Many wasps and bees learn the position of their nest relative to nearby visual features during elaborate 'learning' flights that they perform on leaving the nest. Return flights to the nest are thought to be patterned so that insects can reach their nest by matching their current view to views of their surroundings stored during learning flights. To understand how ground-nesting bumblebees might implement such a matching process, we have video-recorded the bees' learning and return flights and analysed the similarities and differences between the principal motifs of their flights. Loops that take bees away from and bring them back towards the nest are common during learning flights and less so in return flights. Zigzags are more prominent on return flights. Both motifs tend to be nest based. Bees often both fly towards and face the nest in the middle of loops and at the turns of zigzags. Before and after flight direction and body orientation are aligned, the two diverge from each other so that the nest is held within the bees' fronto-lateral visual field while flight direction relative to the nest can fluctuate more widely. These and other parallels between loops and zigzags suggest that they are stable variations of an underlying pattern, which enable bees to store and reacquire similar nest-focused views during learning and return flights.

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. Bees are thus free within limits to adjust their viewing direction relative to the nest, without disturbing flight direction. Second, we examine the coordination of nest-based and compass-based control during likely information gathering segments of these flights: loops during learning flights and zigzags on return flights. We find that bees tend to start a loop or zigzag when flying within a restricted range of compass directions and to fly towards the nest and face it after a fixed change in compass direction, without continuous interactions between their nest-based and compass-based directions of flight. A preferred trajectory of compass-based flight over the course of a motif, combined with the tendency of the bees to keep their body oriented towards the nest automatically narrows the range of compass directions over which bees view the nest. Additionally, the absence of interactions between the two reference frames allows loops and zigzags to have a stereotyped form that can generate informative visual feedback.