Sub-cell scale features govern the placement of new cells by honeybees during comb construction.

Honeybee comb architecture and the manner of its construction have long been the subject of scientific curiosity. Comb is characterised by an even hexagonal layout and the sharing of cell bases and side walls, which provides maximised storage volume while requiring minimal wax. The efficiency of this structure relies on a regular layout and the correct positioning of cells relative to each other, with each new cell placed at the junction of two previously constructed cells. This task is complicated by the incomplete nature of cells at the edge of comb, where new cells are to be built. We presented bees with wax stimuli comprising shallow depressions and protuberances in simulation of features found within partially formed comb, and demonstrated that construction work by honeybee builders was influenced by these stimuli. The building of new cells was aligned to concave stimuli that simulated the clefts that naturally appear between two partially formed cells, revealing how new cells may be aligned to ensure proper tessellation within comb. We also found that bees built cell walls in response to edges formed by our stimuli, suggesting that cell and wall construction was specifically directed towards the locations necessary for continuation of hexagonal comb.

Bumblebees acquire alternative puzzle-box solutions via social learning.

The astonishing behavioural repertoires of social insects have been thought largely innate, but these insects have repeatedly demonstrated remarkable capacities for both individual and social learning. Using the bumblebee Bombus terrestris as a model, we developed a two-option puzzle box task and used open diffusion paradigms to observe the transmission of novel, nonnatural foraging behaviours through populations. Box-opening behaviour spread through colonies seeded with a demonstrator trained to perform 1 of the 2 possible behavioural variants, and the observers acquired the demonstrated variant. This preference persisted among observers even when the alternative technique was discovered. In control diffusion experiments that lacked a demonstrator, some bees spontaneously opened the puzzle boxes but were significantly less proficient than those that learned in the presence of a demonstrator. This suggested that social learning was crucial to proper acquisition of box opening. Additional open diffusion experiments where 2 behavioural variants were initially present in similar proportions ended with a single variant becoming dominant, due to stochastic processes. We discuss whether these results, which replicate those found in primates and birds, might indicate a capacity for culture in bumblebees.

Discrimination of edge orientation by bumblebees.

Simple feature detectors in the visual system, such as edge-detectors, are likely to underlie even the most complex visual processing, so understanding the limits of these systems is crucial for a fuller understanding of visual processing. We investigated the ability of bumblebees (Bombus terrestris) to discriminate between differently angled edges. In a multiple-choice, "meadow-like" scenario, bumblebees successfully discriminated between angled bars with 7° differences, significantly exceeding the previously reported performance of eastern honeybees (Apis cerana, limit: 15°). Neither the rate at which bees learned, nor their final discrimination performance were affected by the angular orientation of the training bars, indicating a uniform performance across the visual field. Previous work has found that, in dual-choice tests, eastern honeybees cannot reliably discriminate between angles with less than 25° difference, suggesting that performance in discrimination tasks is affected by the training regime, and doesn't simply reflect the perceptual limitations of the visual system. We used high resolution LCD monitors to investigate bumblebees' angular resolution in a dual-choice experiment. Bumblebees could still discriminate 7° angle differences under such conditions (exceeding the previously reported limit for Apis mellifera, of 10°, as well as that of A. cerana). Bees eventually reached similar levels of accuracy in the dual-choice experiment as they did under multiple-choice conditions but required longer learning periods. Bumblebees show impressive abilities to discriminate between angled edges, performing better than two previously tested species of honeybee. This high performance may, in turn, support complex visual processing in the bumblebee brain.

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.

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

Male 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.

Harmonic radar tracking reveals random dispersal pattern of bumblebee (Bombus terrestris) queens after hibernation.

The dispersal of animals from their birth place has profound effects on the immediate survival and longer-term persistence of populations. Molecular studies have estimated that bumblebee colonies can be established many kilometers from their queens' natal nest site. However, little is known about when and how queens disperse during their lifespan. One possible life stage when dispersal may occur, is directly after emerging from hibernation. Here, harmonic radar tracking of artificially over-wintered Bombus terrestris queens shows that they spend most of their time resting on the ground with intermittent very short flights (duration and distance). We corroborate these behaviors with observations of wild queen bees, which show similar prolonged resting periods between short flights, indicating that the behavior of our radar-monitored bees was not due to the attachment of transponders nor an artifact of the bees being commercially reared. Radar-monitored flights were not continuously directed away from the origin, suggesting that bees were not intentionally trying to disperse from their artificial emergence site. Flights did not loop back to the origin suggesting bees were not trying to remember or get back to the original release site. Most individuals dispersed from the range of the harmonic radar within less than two days and did not return. Flight directions were not different from a uniform distribution and flight lengths followed an exponential distribution, both suggesting random dispersal. A random walk model based on our observed data estimates a positive net dispersal from the origin over many flights, indicating a biased random dispersal, and estimates the net displacement of queens to be within the range of those estimated in genetic studies. We suggest that a distinct post-hibernation life history stage consisting mostly of rest with intermittent short flights and infrequent foraging fulfils the dual purpose of ovary development and dispersal prior to nest searching.

Continuous Radar Tracking Illustrates the Development of Multi-destination Routes of Bumblebees.

Animals that visit multiple foraging sites face a problem, analogous to the Travelling Salesman Problem, of finding an efficient route. We explored bumblebees' route development on an array of five artificial flowers in which minimising travel distances between individual feeders conflicted with minimising overall distance. No previous study of bee spatial navigation has been able to follow animals' movement during learning; we tracked bumblebee foragers continuously, using harmonic radar, and examined the process of route formation in detail for a small number of selected individuals. On our array, bees did not settle on visit sequences that gave the shortest overall path, but prioritised movements to nearby feeders. Nonetheless, flight distance and duration reduced with experience. This increased efficiency was attributable mainly to experienced bees reducing exploration beyond the feeder array and flights becoming straighter with experience, rather than improvements in the sequence of feeder visits. Flight paths of all legs of a flight stabilised at similar rates, whereas the first few feeder visits became fixed early while bees continued to experiment with the order of later visits. Stabilising early sections of a route and prioritising travel between nearby destinations may reduce the search space, allowing rapid adoption of efficient routes.

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.

Life-Long Radar Tracking of Bumblebees.

Insect pollinators such as bumblebees play a vital role in many ecosystems, so it is important to understand their foraging movements on a landscape scale. We used harmonic radar to record the natural foraging behaviour of Bombus terrestris audax workers over their entire foraging career. Every flight ever made outside the nest by four foragers was recorded. Our data reveal where the bees flew and how their behaviour changed with experience, at an unprecedented level of detail. We identified how each bee's flights fit into two categories-which we named exploration and exploitation flights-examining the differences between the two types of flight and how their occurrence changed over the course of the bees' foraging careers. Exploitation of learned resources takes place during efficient, straight trips, usually to a single foraging location, and is seldom combined with exploration of other areas. Exploration of the landscape typically occurs in the first few flights made by each bee, but our data show that further exploration flights can be made throughout the bee's foraging career. Bees showed striking levels of variation in how they explored their environment, their fidelity to particular patches, ratio of exploration to exploitation, duration and frequency of their foraging bouts. One bee developed a straight route to a forage patch within four flights and followed this route exclusively for six days before abandoning it entirely for a closer location; this second location had not been visited since her first exploratory flight nine days prior. Another bee made only rare exploitation flights and continued to explore widely throughout its life; two other bees showed more frequent switches between exploration and exploitation. Our data shed light on the way bumblebees balance exploration of the environment with exploitation of resources and reveal extreme levels of variation between individuals.

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.

Environmental and genetic control of brain and song structure in the zebra finch.

Birdsong is a classic example of a learned trait with cultural inheritance, with selection acting on trait expression. To understand how song responds to selection, it is vital to determine the extent to which variation in song learning and neuroanatomy is attributable to genetic variation, environmental conditions, or their interactions. Using a partial cross fostering design with an experimental stressor, we quantified the heritability of song structure and key brain nuclei in the song control system of the zebra finch and the genotype-by-environment (G × E) interactions. Neuroanatomy and song structure both showed low levels of heritability and are unlikely to be under selection as indicators of genetic quality. HVC, in particular, was almost entirely under environmental control. G × E interaction was important for brain development and may provide a mechanism by which additive genetic variation is maintained, which in turn may promote sexual selection through female choice. Our study suggests that selection may act on the genes determining vocal learning, rather than directly on the underlying neuroanatomy, and emphasizes the fundamental importance of environmental conditions for vocal learning and neural development in songbirds.