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

This is the final version. Available on open access from the Company of Biologists via the DOI in this recordThe 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.University of Susse

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

This is the final version of the article. Available from the publisher via the DOI in this recordInsects 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.Financial support came from the EPSRC, Biotechnology and Biological Sciences Research Council (BBSRC) and The Leverhulme Trust. O.R. was supported by the Overseas Researc

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

Multimodal influences on learning walks in desert ants (Cataglyphis fortis)

Ants are excellent navigators using multimodal information for navigation. To accurately localise the nest at the end of a foraging journey, visual cues, wind direction and also olfactory cues need to be learnt. Learning walks are performed at the start of an ant’s foraging career or when the appearance of the nest surrounding has changed. We investigated here whether the structure of such learning walks in the desert ant Cataglyphis fortis takes into account wind direction in conjunction with the learning of new visual information. Ants learnt to travel back and forth between their nest and a feeder, and we then introduced a black cylinder near their nest to induce learning walks in regular foragers. By doing this across days with different wind directions, we were able to probe how ants balance different sensory modalities. We found that (1) the ants’ outwards headings are influenced by the wind direction with their routes deflected such that they will arrive downwind of their target, (2) a novel object along the route induces learning walks in experienced ants and (3) the structure of learning walks is shaped by the wind direction rather than the position of the visual cue

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

Notes (pdf), data (Matlab)The article associated with this dataset is available in ORE at: http://hdl.handle.net/10871/132859The 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. Bumblebees like many other bees, wasps and ants learn views of their nest surroundings while they face their nest. We find 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 significance of the coordinated manoeuvre is apparent during return flights after foraging. Bees then adopt a similar preferred body-orientation when they are close to the nest. How does a bee, unacquainted with its surroundings, know when it is facing its nest? A likely answer is path integration which gives bees continuously updated information about the current direction of their nest. Path integration also enables bees to fixate the nest when the body points in the appropriate 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 adopting a preferred body orientation and flight direction within the visual surroundings of the nest are geocentric.Engineering and Physical Sciences Research Council (EPSRC)Leverhulme TrustLeverhulme Trus

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

This is the author accepted manuscript. The final version is available on open access from the Company of Biologists via the DOI in this recordThe dataset associated with this article is available in ORE at https://doi.org/10.24378/exe.4606The 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. Bumblebees like many other bees, wasps and ants learn views of their nest surroundings while they face their nest. We find 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 significance of the coordinated manoeuvre is apparent during return flights after foraging. Bees then adopt a similar preferred body-orientation when they are close to the nest. How does a bee, unacquainted with its surroundings, know when it is facing its nest? A likely answer is path integration which gives bees continuously updated information about the current direction of their nest. Path integration also enables bees to fixate the nest when the body points in the appropriate 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 adopting a preferred body orientation and flight direction within the visual surroundings of the nest are geocentric.Leverhulme TrustEngineering and Physical Sciences Research Council (EPSRC

Bioacoustics and biophysical analysis of a newly described highly transparent genus of predatory katydids from the Andean cloud forest (Orthoptera: Tettigoniidae: Meconematinae: Phlugidini)

Transparency is a greatly advantageous form of camouflage, allowing species to passively avoid detection regardless of the properties of the surface which they occupy. However, it is uncommon and poorly understood in terrestrial species. In one tribe of predacious katydids (Phlugidini), transparency is paired with highly ultrasonic communication for increased predator evasion, yet little is known about the singing capabilities of these species, with only one genus of Phlugidini acoustically well described to date. Here, we describe Speculophlugis hishquten new genus and species of highly transparent crystal katydid species from the Andean cloud forest, discussing the potential use of this species for non-invasive studies of internal anatomy, and analysing its ultrasonic call. Using laser Doppler vibrometry and light microscopy techniques, we found the transparency of the cuticle around the hearing apparatus to be 85-87 % at the wavelength of the laser beam (633 nm), making S. hishquten a candidate for the highest recorded cuticle transparency of any insect. The male song has a fundamental frequency of 50 kHz, matching both the ultrasonic call range and rapid call structure of other Phlugidini species. However, the extent of ultrasonic communication and the level of transparency across the Phlugidini tribe requires more attention

The Typical Flight Performance of Blowflies: Measuring the Normal Performance Envelope of Calliphora vicina Using a Novel Corner-Cube Arena

Despite a wealth of evidence demonstrating extraordinary maximal performance, little is known about the routine flight performance of insects. We present a set of techniques for benchmarking performance characteristics of insects in free flight, demonstrated using a model species, and comment on the significance of the performance observed. Free-flying blowflies (Calliphora vicina) were filmed inside a novel mirrored arena comprising a large (1.6 m1.6 m1.6 m) corner-cube reflector using a single high-speed digital video camera (250 or 500 fps). This arrangement permitted accurate reconstruction of the flies' 3-dimensional trajectories without the need for synchronisation hardware, by virtue of the multiple reflections of a subject within the arena. Image sequences were analysed using custom-written automated tracking software, and processed using a self-calibrating bundle adjustment procedure to determine the subject's instantaneous 3-dimensional position. We illustrate our method by using these trajectory data to benchmark the routine flight performance envelope of our flies. Flight speeds were most commonly observed between 1.2 ms−1 and 2.3 ms−1, with a maximum of 2.5 ms−1. Our flies tended to dive faster than they climbed, with a maximum descent rate (−2.4 ms−1) almost double the maximum climb rate (1.2 ms−1). Modal turn rate was around 240°s−1, with maximal rates in excess of 1700°s−1. We used the maximal flight performance we observed during normal flight to construct notional physical limits on the blowfly flight envelope, and used the distribution of observations within that notional envelope to postulate behavioural preferences or physiological and anatomical constraints. The flight trajectories we recorded were never steady: rather they were constantly accelerating or decelerating, with maximum tangential accelerations and maximum centripetal accelerations on the order of 3 g

Distinct Visual Working Memory Systems for View-Dependent and View-Invariant Representation

Background: How do people sustain a visual representation of the environment? Currently, many researchers argue that a single visual working memory system sustains non-spatial object information such as colors and shapes. However, previous studies tested visual working memory for two-dimensional objects only. In consequence, the nature of visual working memory for three-dimensional (3D) object representation remains unknown. Methodology/Principal Findings: Here, I show that when sustaining information about 3D objects, visual working memory clearly divides into two separate, specialized memory systems, rather than one system, as was previously thought. One memory system gradually accumulates sensory information, forming an increasingly precise view-dependent representation of the scene over the course of several seconds. A second memory system sustains view-invariant representations of 3D objects. The view-dependent memory system has a storage capacity of 3–4 representations and the view-invariant memory system has a storage capacity of 1–2 representations. These systems can operate independently from one another and do not compete for working memory storage resources. Conclusions/Significance: These results provide evidence that visual working memory sustains object information in two separate, specialized memory systems. One memory system sustains view-dependent representations of the scene, akin to the view-specific representations that guide place recognition during navigation in humans, rodents and insects. Th