Ground-nesting bees determine the location of their nest relative to a landmark by other than angular size cues

Bees and wasps acquire a visual representation of their nest's environment and use it to locate their nest when they return from foraging trips. This representation contains among other features cues to the distance of near-by landmarks. We worked with two species of ground-nesting bees, Lasioglossum malachurum (Hymenoptera: Halictidae), Dasypoda hirtipes (Hymenoptera: Melittidae) and asked which cues to landmark distance they use during homing. Bees learned to associate a single cylindrical landmark with their nest's location. We subsequently tested returning bees with landmarks of different sizes and thus introduced large discrepancies between the angular size of the landmark as seen from the nest during training and its distance from the nest. The bees' search behaviour and their choice of dummy nest entrances show that both species of ground-nesting bees consistently search for their nest at the learned distance from landmarks. The influence of the apparent size of landmarks on the bees' search and choice behaviour is comparatively weak. We suggest that the bees exploit cues derived from the apparent speed of the landmark's image at their retina for distance evaluation.     

Garden ant homing behavior in a maze task based on local visual cues

Although it has been shown that visual cues play an essential role in navigation by the garden ant Lasius niger, no previous studies have addressed the way in which information from local visual cues is acquired and utilized in navigation. We found that in the absence of pheromone trails, ants whose homing motivation was triggered by feeding returned to the nest following local visual cues. In our experiments, the ants travelled through a maze to reach a feeder. They explored the maze and sometimes became trapped in its dead ends. We found that the ants more effectively used visual cues during their homeward journey if they experienced a dead end during their outward journey. This result suggested that the ants used the information acquired from visual cues during the outward journey to avoid a dead end on their return journey.     

Nocturnal Homing: Learning Walks in a Wandering Spider?

Homing by the nocturnal Namib Desert spider Leucorchestris arenicola (Araneae: Sparassidae) is comparable to homing in diurnal bees, wasps and ants in terms of path length and layout. The spiders'' homing is based on vision but their basic navigational strategy is unclear. Diurnal homing insects use memorised views of their home in snapshot matching strategies. The insects learn the visual scenery identifying their nest location during learning flights (e.g. bees and wasps) or walks (ants). These learning flights and walks are stereotyped movement patterns clearly different from other movement behaviours. If the visual homing of L. arenicola is also based on an image matching strategy they are likely to exhibit learning walks similar to diurnal insects. To explore this possibility we recorded departures of spiders from a new burrow in an unfamiliar area with infrared cameras and analysed their paths using computer tracking techniques. We found that L. arenicola performs distinct stereotyped movement patterns during the first part of their departures in an unfamiliar area and that they seem to learn the appearance of their home during these movement patterns. We conclude that the spiders perform learning walks and this strongly suggests that L. arenicola uses a visual memory of the burrow location when homing.     

Contextual modulation of visuomotor associations in bumble-bees (Bombus terrestris)

We performed the following experiment to investigate whether contextual cues can prevent interference during the acquisition of potentially competing visuomotor associations. In the bumble-bee (Bombus terrestris). Bees discriminated between horizontally and vertically orientated gratings of black and white stripes in order to reach a feeder and between different diagonally orientated gratings to gain access to their nest. Once bees were well trained on these two tasks, the discrimination task at the nest was changed so that bees had to distinguish between horizontal and vertical gratings at both sites. Whereas they still approached the horizontal grating to reach food, they now had to approach a vertical grating in order to return to their nest. The new task was learnt rapidly. Errors at the feeder did not increase during or after the acquisition of this potentially competing behaviour at the nest entrance. For a brief period during acquisition, bees showed some hesitation at the feeder and hovered for slightly longer before choosing between horizontals and verticals. After acquisition was complete, bees showed a slight increase in their preference for verticals over a more ambiguous stimulus of an array of dots. These findings are consistent with the hypothesis that different contextual signals are associated with approaching the nest or approaching the feeder, and that these contextual signals facilitate learnt associations between orientation detectors and motor commands.     

Individual scent marking of the nest entrance as a mechanism for nest recognition inXylocopa pubescens (Hymenoptera: Anthophoridae)

The mechanism by which female Xylocopa pubescenslocate their nest in a nesting aggregation was investigated. The bees were induced to nest in canes to which uniform nest entrances were attached. The results of nest displacement experiments revealed that the bees use visual cues for proximate orientation,but at very close range they also use olfactory cues. This conclusion was corroborated by the results of experiments in which the nest entrances were either removed or exchanged for alien nest entrances. Moreover, habituation experiments strongly indicated that the bees impart their individual marking at the nest entrance and that they can learn and memorize the individual odors of the neighboring bees.     

Landmark orientation during the approach to the nest in the stingless beeTrigona (Tetragonisca) angustula (Apidae,Meliponinae)

Summary We displaced a small nest box containing stingless bees (Trigona (Tetragonisca)angustula) over distances of up to 1.6 meters in different directions and counted the numbers of returning foragers to measure the effects of this manipulation on the homing ability of bees. Bees find it hard to locate the nest box when it was displaced more than about 1 m backwards, forwards or sideways relative to the direction into which the nest entrance pointed. They do not find the nest when its height above ground is changed. The bees use landmarks in the vicinity of the nest to locate it: When the nest box is displaced and landmark positions are changed so that their angular position at the new nest site is the same as at the normal nest position their homing ability is less impaired than it is without changes in landmark positions. Our results show that the bees do not use the nest box itself as a landmark until they have approached the nest position to within about 1 meter with the aid of surrounding landmarks.     

Visual Navigation during Colony Emigration by the Ant Temnothorax rugatulus

Many ants rely on both visual cues and self-generated chemical signals for navigation, but their relative importance varies across species and context. We evaluated the roles of both modalities during colony emigration by Temnothorax rugatulus. Colonies were induced to move from an old nest in the center of an arena to a new nest at the arena edge. In the midst of the emigration the arena floor was rotated 60°around the old nest entrance, thus displacing any substrate-bound odor cues while leaving visual cues unchanged. This manipulation had no effect on orientation, suggesting little influence of substrate cues on navigation. When this rotation was accompanied by the blocking of most visual cues, the ants became highly disoriented, suggesting that they did not fall back on substrate cues even when deprived of visual information. Finally, when the substrate was left in place but the visual surround was rotated, the ants'' subsequent headings were strongly rotated in the same direction, showing a clear role for visual navigation. Combined with earlier studies, these results suggest that chemical signals deposited by Temnothorax ants serve more for marking of familiar territory than for orientation. The ants instead navigate visually, showing the importance of this modality even for species with small eyes and coarse visual acuity.     

Navigation without vision: bumblebee orientation in complete darkness

In flight cages, worker bumblebees (Bombus impatiens) spontaneously explored the surroundings of their nest and foraged in complete darkness, by walking instead of flying, from feeders up to 150 cm away from the nest. This behaviour was wholly unexpected in these classically visual foragers. The finding provides a controlled system for dissecting possible non-visual components of navigation used in daylight. It also allows us to isolate navigation mechanisms used in naturally dark situations, such as in the nest. Using infrared video, we mapped walking trails. We found that bumblebees laid odour marks. When such odour cues were eliminated, bees maintained correct directionality, suggesting a magnetic compass. They were also able to assess travel distance correctly, using an internal, non-visual, measure of path length. Path integration was not employed. Presumably, this complex navigational skill requires visual input in bees.     

An edge-detection approach to investigating pigeon navigation

This study brings together work in pattern recognition and animal behaviour. By applying algorithms in pattern recognition, we examined how visual landscape information influences pigeons' homing behaviour. We used an automated procedure (Canny edge detector) to extract edges from an aerial image of the experimental terrain. Analysis of pigeons' homing routes recorded using global positioning system (GPS) trackers showed that the chosen homing paths, as well as changes in the birds' navigational states, tended to coincide with these edges. This study demonstrates that some edge-containing land features attract homing pigeons and trigger changes in their navigational states.     

Conditions for landmark-based navigation in the house mouse, Mus musculus

I investigated whether mice, after learning to home by relying on visual extra-arena landmarks, still required instantaneous access to such cues for successful navigation. Two groups of lactating mice were trained to retrieve their pups from the centre of a circular arena back to their peripheral nest. On test trials, mice from one group were allowed to view distal visual cues while moving from the nest towards the centre, and mice from the other group were allowed to view distal visual cues when homing from the centre towards the nest. The results indicate that viewing the visual cues when homing is necessary for landmark-based navigation.     

Distinguishing signals and cues: bumblebees use general footprints to generate adaptive behaviour at flowers and nest

Chemicals used in communication are divided into signals and cues. Signals are moulded by natural selection to carry specific meanings in specific contexts. Cues, on the other hand, have not been moulded by natural selection to carry specific information for intended receivers. Distinguishing between these two modes of information transfer is difficult when animals do not perform obvious secretion behaviours. Although a number of insects have been suspected of leaving cues at food sites and nest entrances, studies have not attempted to experimentally distinguish between cues and signals. Here, we examine the chemical composition of the scent marks left by the bumblebee Bombus terrestris at food sites and compare it to those found at a neutral location. If bees are depositing a cue, we expect the same chemicals to be found at both sites, but if they deposit a signal we only expect to find the scent marks at the food site. We were also interested in identifying the chemicals left at the nest entrance to determine if they differed from those used to mark food sites. We find that bees deposit the same chemicals at food, nest and neutral sites. Therefore, bumblebees leave behind general chemical footprints everywhere they walk and we propose that they learn to use these footprints in a manner that ultimately enhances their fitness, for example, to improve their foraging efficiency and locate their nest. Experimentally, distinguishing these two modes of information transfer is crucial for understanding how they interact to shape animal behaviour and what chemical bouquets are under natural selection. Handling Editor: Heikki Hokkanen     

Experience Based Use of Landmark and Vector Based Orientation During Homing by the Ant Formica cunicularia (Hymenoptera: Formicidae)

Homing paths of Formica cunicularia foragers from an artificial food reward were analyzed on a familiar terrain and in displacement experiments on a familiar and an unfamiliar terrain. Foragers were tested either when relatively new to a foraging route (untrained group) or after a day’s experience with it (trained group). Untrained foragers followed direct homing paths to the nest site when tested in the familiar terrain but followed tortuous paths when displaced to the unfamiliar terrain. Trained foragers behaved similarly to untrained ones when tested from the food reward to the nest site in the familiar terrain but their behavior changed in displacements. Irrespective of the familiarity of the displacement site, these foragers followed paths taking them to the expected nest sites. The results showed that foragers did not rely on chemical cues for homing and revealed that untrained foragers disregarded path integration and were directed to the nest site when it is in their visual panorama. On the contrary, trained foragers may have relied on path integration on familiar and unfamiliar terrain. The results also demonstrated that experience greatly affected the preferential use of visual and vector based cues by foragers during homing.     

Distance estimation in the third dimension in desert ants

Desert ants of the genus Cataglyphis perform large-scale foraging excursions from which they return to their nest by path integration. They do so by integrating courses steered and the distances travelled into a continually updated home vector. While it is known that the angular orientation is based on skylight cues, it still is largely enigmatic how the ants measure distances travelled. We extended the ants' task into the third dimension by training them to walk within an array of uphill and downhill channels, and later testing them on flat terrain, or vice versa. In these tests the ants indicated homing distances that did not correspond to the distances actually travelled, but to the ground distances; that is, to the sum of the horizontal projections of the uphill and downhill segments of the ants' paths. These results suggest a much more sophisticated mechanism of distance estimation than hitherto thought. The ants must be able to measure the slopes of undulating terrain and to integrate this information into their "odometer" for the distance estimation process.     

A stingless bee (Melipona seminigra) uses optic flow to estimate flight distances

Foragers of a stingless bee, Melipona seminigra, are able to use the optic flow experienced en route to estimate flight distance. After training the bees to collect food inside a flight tunnel with black-and-white stripes covering the side walls and the floor, their search behavior was observed in tunnels lacking a reward. Like honeybees, the bees accurately estimated the distance to the previously offered food source as seen from the sections of the tunnel where they turned around in search of the food. Changing the visual flow by decreasing the width of the flight tunnel resulted in the underestimation of the distance flown. The removal of image motion cues either in the ventral or lateral field of view reduced the bees' ability to gauge distances. When the feeder inside the tunnel was displaced together with the bees feeding on it while preventing the bee from seeing any image motion during the displacement the bees experienced different distances on their way to the food source and during their return to the nest. In the subsequent test the bees searched for the food predominantly at the distance associated with their return flight.     

Recognition of a familiar place by the honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Recent work shows that at any one place bees detect a limited variety of simple cues in parallel. At each choice point, they recognize a few cues in the range of positions where the cues occurred during the learning process. There is no need to postulate that they re-assemble the surrounding panorama in memory; only that they retain memories of the coincidences of cues in the expected retinotopic directions. The cues could be stimuli that excite groups of peripheral visual neurons. All the experimentally known cues are described, including modulation of the receptors, the locations of areas of black or colour, the nearness, size, averaged edge orientation, and radial and tangential edges. Cues of each type are separately summed within large fields, the size of which varies with the cue. Local orientation cues from edges at right angles cancel each other within each field, which also suggests that the discrimination of shape and texture is limited. Resolution depends on lateral interactions and the number of ommatidia required for each cue. To identify a new place, a few sparse cues, together with their directions, are learned in orientation flights. When the bee returns, the cues in the panorama are progressively matched as they coincide with the cues in memory. The limited number of cues, though economical for memory, may restrict the foraging behaviour and lead to flower constancy. This kind of a visual system is a candidate model for other animals or machines with economical processing systems.     

Path integration controls nest-plume following in desert ants

The desert ant Cataglyphis fortis is equipped with sophisticated navigational skills for returning to its nest after foraging. The ant's primary means for long-distance navigation is path integration, which provides a continuous readout of the ant's approximate distance and direction from the nest. The nest is pinpointed with the aid of visual and olfactory landmarks. Similar landmark cues help ants locate familiar food sites. Ants on their outward trip will position themselves so that they can move upwind using odor cues to find food. Here we show that homing ants also move upwind along nest-derived odor plumes to approach their nest. The ants only respond to odor plumes if the state of their path integrator tells them that they are near the nest. This influence of path integration is important because we could experimentally provoke ants to follow odor plumes from a foreign, conspecific nest and enter that nest. We identified CO(2) as one nest-plume component that can by itself induce plume following in homing ants. Taken together, the results suggest that path-integration information enables ants to avoid entering the wrong nest, where they would inevitably be killed by resident ants.     

Large scale homing in honeybees

Honeybee foragers frequently fly several kilometres to and from vital resources, and communicate those locations to their nest mates by a symbolic dance language. Research has shown that they achieve this feat by memorizing landmarks and the skyline panorama, using the sun and polarized skylight as compasses and by integrating their outbound flight paths. In order to investigate the capacity of the honeybees' homing abilities, we artificially displaced foragers to novel release spots at various distances up to 13 km in the four cardinal directions. Returning bees were individually registered by a radio frequency identification (RFID) system at the hive entrance. We found that homing rate, homing speed and the maximum homing distance depend on the release direction. Bees released in the east were more likely to find their way back home, and returned faster than bees released in any other direction, due to the familiarity of global landmarks seen from the hive. Our findings suggest that such large scale homing is facilitated by global landmarks acting as beacons, and possibly the entire skyline panorama.     

Seeing is believing: information content and behavioural response to visual and chemical cues

Predator avoidance and foraging often pose conflicting demands. Animals can decrease mortality risk searching for predators, but searching decreases foraging time and hence intake. We used this principle to investigate how prey should use information to detect, assess and respond to predation risk from an optimal foraging perspective. A mathematical model showed that solitary bees should increase flower examination time in response to predator cues and that the rate of false alarms should be negatively correlated with the relative value of the flower explored. The predatory ant, Oecophylla smaragdina, and the harmless ant, Polyrhachis dives, differ in the profile of volatiles they emit and in their visual appearance. As predicted, the solitary bee Nomia strigata spent more time examining virgin flowers in presence of predator cues than in their absence. Furthermore, the proportion of flowers rejected decreased from morning to noon, as the relative value of virgin flowers increased. In addition, bees responded differently to visual and chemical cues. While chemical cues induced bees to search around flowers, bees detecting visual cues hovered in front of them. These strategies may allow prey to identify the nature of visual cues and to locate the source of chemical cues.     

The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees

Traditional models of insect vision have assumed that insects are only capable of low-level analysis of local cues and are incapable of global, holistic perception. However, recent studies on honeybee (Apis mellifera) vision have refuted this view by showing that this insect also processes complex visual information by using spatial configurations or relational rules. In the light of these findings, we asked whether bees prioritize global configurations or local cues by setting these two levels of image analysis in competition. We trained individual free-flying honeybees to discriminate hierarchical visual stimuli within a Y-maze and tested bees with novel stimuli in which local and/or global cues were manipulated. We demonstrate that even when local information is accessible, bees prefer global information, thus relying mainly on the object''s spatial configuration rather than on elemental, local information. This preference can be reversed if bees are pre-trained to discriminate isolated local cues. In this case, bees prefer the hierarchical stimuli with the local elements previously primed even if they build an incorrect global configuration. Pre-training with local cues induces a generic attentional bias towards any local elements as local information is prioritized in the test, even if the local cues used in the test are different from the pre-trained ones. Our results thus underline the plasticity of visual processing in insects and provide new insights for the comparative analysis of visual recognition in humans and animals.     

Long-distance Homing Ability in Dasypoda altercator (Hymenoptera,Melittidae)

Homing rates and initial orientations after release from different directions were investigated in the solitary bee Dasypoda altercator. Homing rates and the proportion of individuals returning on the day of release declined with distance, implying that homing from greater distances is not based solely on the use of landmarks. A long duration of return (often not on the same day) and high efficiency of homing (four bees out of 10 returned from a 4 km distance over the lake), as well as an increase in average return speed ? 10 m/min) with distance of bees homing on the same day suggest that homing is also not based upon radial scatter as the sole tactic. This is supported by the observation that the initial orientations of the bees were not equally probable. Departures towards the sun greatly exceeded those away from the sun and the bees also tended to depart in cardinal geographical (or geomagnetic) directions, preferring meridional directions (especially southward) to parallel ones (of which east was preferred). Departure directions did not depend on wind direction but did depend, to some extent, on the landscape features of release sites. However, bees neither tended to depart in the direction of the nest, nor did homing success correlate with the direction of departure in relation to that of the nest.