Approaching and departing bees learn different cues to the distance of a landmark

Bees learn both the absolute distance and the apparent size of landmarks in the vicinity of a foraging site. They learn about landmarks both when approaching and when leaving the site. Whereas learning on arrival can take place on every visit to the food source, learning on departure is limited to the first few visits, when the bee Turns Back and Looks (TBL) at the feeder in a stereotyped manoeuvre before flying off. We investigated whether one specific function of TBLs is to acquire information about the absolute distance of landmarks from the feeding site. Bees were trained to forage from a feeder which lay at a fixed distance from a cylinder. During training, bees were exposed to the cylinder either only while they approached and landed on the feeder, or only on their departure from it, or at both of these times. Tests on trained bees immediately after the TBL phase revealed that those bees which had viewed the cylinder only on arrival had learnt the apparent size of the cylinder, but not its distance from the feeder. In contrast, bees which saw the cylinder on departure had learnt its absolute distance. They also learnt the cylinder's apparent size, provided that the cylinder was close to the feeder. Bees which had viewed the cylinder on arrival as well as on departure learnt both absolute distance and apparent size. Distance dominated the bees' behaviour in the initial phase of learning, apparent size was more important later on. We suggest that early during learning bees need information about the 3-D structure of the environment so that they can identify those landmarks close to a foraging site which will specify accurately the site's position. This information is acquired during TBLs. Later, landmark guidance can be achieved by 2-D image matching.     

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.     

Nest site preference and success in a gregarious, ground-nesting bee Dieunomia triangulifera

1. The characteristics of preferred nest sites of the solitary bee Dieunomia triangulifera, which nests gregariously in alluvial soil, were investigated. Nest presence was used as an indication of preference. In those cases where nests were more than a few days old, therefore, this study also investigated nest success. 2. Independent variables tested were soil surface moisture, presence of nesting conspecifics, smooth vs. irregular soil surface, distance to visual landmarks, percentage of vegetation cover, soil compaction, vehicular traffic, soil surface temperature, and light intensity. 3. Bees preferred to nest in moist, compact soil with an irregular surface. More bees nested near visual landmarks and in places with little or no vegetation. They preferred nesting in areas with warmer soil surface temperatures and brighter illumination. The presence of nesting conspecifics did not influence nesting decisions. Vehicular traffic also seemed to have no impact on nest initiation but did seem to have a negative impact on nest success. 4. Although it might seem that ground-nesting bees should not be limited by nesting sites, relatively little of the study area met all their apparent criteria. This might account, in part, for gregarious nesting in this species.     

Orientation flights of solitary wasps (Cerceris; Sphecidae; Hymenoptera)

Bees and wasps are known to use a visual representation of the nest environment to guide the final approach to their nest. It is also known that they acquire this representation during an orientation flight performed on departure.A detailed film analysis shows that orientation flights in solitary wasps of the genus Cerceris consist of a systematic behavioural sequence: after lift-off from the nest entrance, wasps fly in ever increasing arcs around the nest. They fly along these arcs obliquely to their long axis and turn so that the nest entrance is held in the left or right visual field at retinal positions between 30° and 70° from the midline. Horizontal distance from the nest and height above ground increase throughout an orientation flight so that the nest is kept at retinal elevations between 45° and 60° below the horizon. The wasps' rate of turning is constant at between 100°/s and 200°/s independent of their distance from the nest and their ground velocity increases with distance. The consequence of this is that throughout the flight wasps circle at a constant angular velocity around the nest.Orientation flights are strongly influenced by landmark lay-out. Wasps adjust their flight-path and their orientation in a way that allows them to fixate the nest entrance and to hold the closest landmark in their frontal visual field.The orientation flight generates a specific topography of motion parallax across the visual field. This could be used by wasps to acquire a series of snapshots that all contain the nest position, to acquire snapshots of close landmarks only (distance filtering), to exclude shadow contours from their visual representation (figure-ground discrimination) or to gain information on the distance of landmarks relative to the nest.     

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.     

Visual marks learned by the solitary bee Megachile rotundata for localizing its nest

We studied homing behaviour of leaf-cutter bees, Megachile rotundata, by using artificial landmarks. We evaluated their nest-searching behaviour in different test situations to elucidate the nature of the visual marks they used in this task. When we modified or removed geometrical figures surrounding the nest, the bees searched for longer, showing that they noticed the introduced changes. However, these manipulations never prevented bees from finding their nest, suggesting that other visual cues were crucial in the task. Manipulations of the edges provided by the boundaries of the device (nest block, metal sheet on which the block was mounted) strongly impaired the homing performance. The further away the edges that were left intact, the stronger was the impairment of the homing behaviour. These results suggest that bees learn the distances of the various edges from the goal and that edges have a hierarchical significance according to their distance from the nest. The most distant edges provide vague information, which suffices to guide the insect towards the next edge in the sequence, until it recognizes the final, precise location of the nest. The results support the conclusion that information on distances is acquired using cues derived from motion parallax generated by the insect's self-motion. Recognition of edge parameters such as position and orientation might be achieved by an image-matching mechanism based on dynamic processes. Thus, in the homing task, there is no clear discrepancy between the eidetic and the parametric hypotheses of spatial representation.     

The retrieval of visuo-spatial memories by honeybees

Summary In order to explore how honeybees manage to retrieve the right landmark-memory in the right place, we trained bees along a short foraging route which consisted of two identical huts 33 m apart. Bees entered each hut to collect a drop of sucrose on the floor. The location of the drop was defined by the same arrangement of four blue and yellow cylindrical landmarks. However, in one hut the drop was between two yellow cylinders and in two other it was to the east of the blue cylinders. On tests with the sucrose missing, bees tended to search in the appropriate area in each hut (Fig. 1), thus showing that they used cues other than the sight of the local landmarks to select the appropriate memory.In a second experiment, the position of the sucrose was specified by yellow cylinders in one hut and by blue triangles in the other. When the arrays were swapped between huts, bees searched in the position specified by the array they encountered (Fig. 2). Thus, memories can be triggered by visual features of local landmarks.Bees were also trained outside to collect food from two platforms 40 m apart. The location of sucrose on one platform was defined by yellow cylinders, and on the other it was defined by blue triangles. When these arrays were exchanged between platforms, bees searched on each platform as though the landmarks had not been swapped. It seems that the more distant surroundings, which fill most of the visual field, may be more potent than the local landmarks in deciding which memory should be retrieved.It is argued that one role of distant landmarks and other contextual cues is to ensure that bees retrieve the correct memory of a constellation of local landmarks while the bees are still some distance away from their goal. Even at a short distance, a bee's current image of local landmarks may differ considerably from its stored representation of those landmarks as seen from the goal. Accurate recall of the appropriate memory will be more certain if it is primed by relatively distant landmarks which present a more constant image as a bee moves in the vicinity of its goal.     

How do insects represent familiar terrain?

We argue here that ants and bees have a piecemeal representation of familiar terrain. These insects remember no more than what is needed to sustain the separate and parallel strategies that they employ when travelling between their nest and foraging sites. One major strategy is path integration. The insect keeps a running tally of its distance and direction from the nest and so can always return home. This global path integration is enhanced by long-term memories of significant sites that insects store in terms of the coordinates (direction and distance) of these sites relative to the nest. With these memories insects can plan routes that are steered by path integration to such sites. Quite distinct from global path integration are memories associated with familiar routes. Route memories include stored views of landmarks along the route with, in some cases, local vectors linked to them. Local vectors by encoding the direction and/or distance from one landmark to the next, or from one landmark to a goal, help an insect keep to a defined route. We review experiments showing that although local vectors can be recalled by recognising landmarks, the global path integration system is independent of landmark information and that landmarks do not have positional coordinates associated with them. The major function of route landmarks is thus procedural, telling an insect what action to perform next, rather than its location relative to the nest.     

Adaptive behaviour of honeybees (Apis mellifera) toward beetle invaders exhibiting various levels of colony integration

Social bees generally host fewer nest invaders than do ants and termites. This is potentially explained by the adaptive defensive strategies of host bees when faced with nest invaders exhibiting various levels of colony integration (based on adaptations to the nest habitat and frequency of nest inhabitation). In the present study, experiments are performed to determine the behaviour at the nest entrance of European honeybee guards Apis mellifera L. (Hymenoptera: Apidae) toward beetle invaders of various levels of behavioural integration into colonies. The species used to test this include Aethina tumida Murray (Coleoptera: Nitidulidae), which is regarded as a highly integrated, unwelcome guest (synechthran) or true guest (symphile); Lobiopa insularis Laporte (Coleoptera: Nitidulidae) and Epuraea luteola Erichson (Coleoptera: Nitidulidae) that are accidentals; and Carpophilus humeralis Fabricius (Coleoptera: Nitidulidae), Carpophilus hemipterus L. (Coleoptera: Nitidulidae) and Tribolium castaneum Herbst (Coleoptera: Tenebrionidae), all of which are species that are not integrated into honeybee colonies. The responses of guard bees to a control bead also are noted. In general, bees ignore T. castaneum and E. luteola to a greater extent than other beetle species. Bees make contact with the black glass bead (a non‐aggressive behaviour) more than they do all beetle species. Bees treat A. tumida more defensively than they treat any other beetle species and the level of bee defensiveness varies by colony. These data suggest an adaptive heightened defensive response by bees toward the most integrated colony intruder but a significantly reduced level of response toward invaders representing all other levels of colony integration.     

Thorax vibrations of a stingless bee (<Emphasis Type="Italic">Melipona seminigra</Emphasis>). I. No influence of visual flow

An important question in stingless bee communication is whether the thorax vibrations produced by foragers of the genus Melipona upon their return to the nest contain spatial information about food sources or not. As previously shown M. seminigra is able to use visual flow to estimate flight distances. The present study investigated whether foraging bees encode the visually measured distance in their thorax vibrations. Bees were trained to collect food in flight tunnels lined with a black-and-white pattern on their side walls and floor, which substantially influenced the image motion they experienced. When the bees had collected inside the tunnels the temporal pattern of their vibrations differed significantly from the pattern after collecting in a natural environment. These changes, however, were not associated with the visual flow experienced inside the tunnel. Bees collecting in tunnels offering little visual flow (stripes parallel to flight direction) modified their vibrations similarly to bees collecting in tunnels with high image motion (cross stripes). A higher energy expenditure due to drastically reduced flight velocities inside the tunnel is suggested to be responsible for changes in the thorax vibrations. The bees' vibrations would thus reflect the overall energetic budget of a foraging trip.     

Alternative Reproductive Strategies of a Gregarious Ground-Nesting Bee, Dieunomia triangulifera (Hymenoptera: Halictidae)

I studied reproductive behavior of females of the gregarious ground-nesting bee Dieunomia triangulifera (Halictidae). During peak bloom of the host plant, Helianthus annuus, some females consistently brought pollen to one nest (provisioning bees), whereas others visited many nests without taking pollen to any (searching bees). Searching bees were more likely to have two or more developed oocytes and crops full of pollen. The ingested pollen probably provided protein for egg production. The differing behavior of provisioning and searching bees combined with contrasting internal morphology, indicated that these two sets of behaviors were alternative reproductive strategies. Three possible explanations for the searching bees' behavior included: usurpation, floating, or intraspecific cleptoparasitism. Each of these is evaluated as a possible function of searching behavior. Given the evidence I conclude that intraspecific cleptoparasitism is the most likely explanation.     

Why do bees turn back and look?

The timing of learning of colour and shape of the food source, as well as of near-by landmarks, was examined exploiting a behaviour described recently, the Turn Back and Look behaviour (TBL): Bees departing from a novel food source after feeding turn around to view it at a short distance (Figs. 2, 3) before departing for the hive. They repeat this behaviour on several successive visits, termed the TBL phase (Fig. 5). To examine the function of the TBL, I trained individual bees in 4 different modes. In the first 3 they could view a food source or a landmark of a particular colour or shape during (i) arrival as well as departure, (ii) only arrival, and (iii) only departure; in the final mode (iv) the bees viewed one colour (or shape) on arrival, and another on departure. At the end of the TBL phase, the bees were tested by offering them a choice between the visual stimulus to which they were trained (modes i–iii) and a different (novel) one, or between the stimulus viewed on arrival and that viewed on departure (mode iv). The test results show that learning after feeding (while performing the TBL), i.e. backward conditioning, occurs regardless of whether the colour (Fig. 6, Fig. 10a) or shape (Fig. 7) of the food source, or the colour (Fig. 10b), shape (Fig. 11), and position (Fig. 12) of a near-by landmark is considered. Bees trained in mode (iv) preferred the stimulus learned on arrival over that learned on departure in almost all cases. However, a stimulus viewed exclusively on departure (mode iii) was often learned as well as when it was viewed exclusively on arrival (mode ii) (Figs. 10a, 11, 12), or both on arrival and departure (mode i) (Fig. 6). The finding that the timing of learning can be manipulated suggests that it is not based on hard wired predispositions to learn particular visual cues on arrival, and others on departure.     

Landmark learning and visuo-spatial memories in gerbils

The aim of this study is to understand what a rodent (Meriones unguiculatus) learns about the geometrical relations between a goal and nearby visual landmarks and how it uses this information to reach a goal. Gerbils were trained to find sunflower seeds on the floor of a light-tight, black painted room illuminated by a single light bulb hung from the ceiling. The position of the seed on the floor was specified by an array of one or more landmarks. Once training was complete, we recorded where the gerbils searched when landmarks were present but the seed was absent. In such tests, gerbils were confronted either with the array of landmarks to which they were accustomed or with a transformation of this array. Animals searched in the appropriate spot when trained to find seeds placed in a constant direction and at a constant distance from a single cylindrical landmark. Since gerbils look in one spot and not in a circle centred on the landmark, the direction between landmark and goal must be supplied by cues external to the landmark array. Distance, on the other hand, must be measured with respect to the landmark. Tests in which the size of the landmark was altered from that used in training suggest that distance is not learned solely in terms of the apparent size of the landmark as seen from the goal. Gerbils can still reach a goal defined by an array of landmarks when the room light is extinguished during their approach. This ability implies that they have already planned a trajectory to the goal before the room is darkened. In order to compute such a trajectory, their internal representation of landmarks and goal needs to contain information about the distances and bearings between landmarks and goal. For planning trajectories, each landmark of an array can be used separately from the others. Gerbils trained to a goal specified by an array of several landmarks were tested with one or more of the landmarks removed or with the array expanded. They then searched as though they had computed an independent trajectory for each landmark. For instance, gerbils trained with an array of two landmarks were tested with the distance between two landmarks doubled. The animals then searched for seeds in two positions, which were at the correct distance and in the right direction from each landmark.(ABSTRACT TRUNCATED AT 400 WORDS)     

Pattern discrimination by the honeybee: disruption as a cue

The discrimination of pattern disruption in freely flying honeybees (Apis mellifera) was examined. Bees were trained to discriminate at a fixed distance between a regularly repeated black/white pattern and the same pattern at a different magnification in targets of the same angular size. The locations of areas of black were regularly shuffled to make them useless as cues. The results of the experiments indicate that the bees discriminate the disruption of the pattern as a whole, irrespective of the actual pattern. Bees trained to prefer a larger period transfer to an even larger period, when given a forced choice with a pair of patterns of differing disruption from those they were trained on, as if their spontaneous preference has not been overcome. Bees trained to prefer a smaller period, however, prefer the former negative pattern rather than transfer to an even smaller period. These results show that the bees do not rely solely on learning the absolute period of a pattern nor the relative disruption of two patterns, and they are confused when these two cues conflict in tests with unfamiliar targets. Bees can discriminate between fields of view that differ in average disruption as a generalized cue, irrespective of pattern. Accepted: 7 April 1997     

Some labels that are recognized on landmarks by the honeybee (Apis mellifera)

Freely flying bees were trained in a situation that resembled the natural task of a bee arriving at a foraging site that was located by a landmark. The bees' task was to locate the reward in the arm of the Y-choice apparatus, where a black pattern on a white background was displayed in one arm versus a white target in the other arm, at a range of 27 cm. The alternative patterns for the training included previously identified cues. They were: an oblique bar, three parallel oblique bars, an oblique grating, a square cross, six spokes, a large or a small spot, a spotty modulation, or a ring. The trained bees were given a variety of interleaved tests to discover the labels they had used to identify the patterns. A label is defined as the coincidence of cues that contributed to the recognition of a single landmark. The bees learned, firstly, the black area at the expected place, secondly, modulation caused by edges at the expected place. These cues were quantified and always available. In addition, the orientation cue was learned from a grating that covered the target, but was ignored in a single bar. The bees learned the positions of the centres of black and of radial symmetry. In tests, they also recognized unfamiliar cues that were not displayed in the training. The cues and preferences were similar to those used to discriminate between two targets. The new experiments validate some old conclusions that have been controversial for 40 years.     

Ant navigation en route to the goal: signature routes facilitate way-finding of Gigantiops destructor

We investigated in laboratory conditions how foragers of the tropical ant Gigantiops destructor develop individually distinctive landmark routes. Way-finding along a familiar route involved the recognition of at least two locations, nest and feeding site, and the representation of spatial relations between these places. Familiar visual landmarks were important both at the beginning and at the end of the foraging journey. A motor routine guided the ants at the start of their foraging path towards the first landmarks, which they learnt to pass consistently on the same side, before taking the next direction. At the last stage of the route, landmark recognition allowed them to pinpoint their preferred feeding site without using distant cues or odometric information. By contrast, ants en route to the goal were not systematically guided by a stereotyped sequence of snapshots recalled at each corresponding stage of the route. Each ant slalomed in an idiosyncratic distinctive way around different midway landmarks from a foraging excursion to the next, which induced a variability of the path shapes in their intermediate parts. By reducing the number of landmark recognition-triggered responses, this economical visuomotor strategy may be helpful in the Amazonian forest where many prominent landmarks are alike.     

Memory and sun compensation by honey bees

Summary Experiments with two species of honey bees (Apis mellifera andA. cerana) have revealed that bees form a detailed memory of the spatial and temporal pattern of the sun's azimuthal movement, using local landmarks as a reference for the learning. These experiments were performed on overcast days, and consisted of removing a hive from one site in which bees had been trained to find food by flying along a prominent landmark, and displacing it to a similar site in which the landmark was aligned in a different compass direction. On overcast days, bees which flew along the landmark in the new site oriented their waggle dances in the hive as if they had actually flown in the training site. Thus, they confused the two sets of landmarks and set their dance angles according to a memory of the sun's position relative to the original landmarks. Furthermore, the dances changed in correspondence with the sun's azimuthal shift over several hours, even reflecting (approximately) the regular temporal variations in the rate of shift; such features of the sun's course must therefore be stored in memory. The primary mechanism underlying the learning of this pattern is probably similar to that proposed by New and New (1962): bees store in memory several time-linked solar azimuthal positions relative to features of the landscape, and refer to this stored array when they need to determine an unknown azimuth intermediate between two known positions.During the cloudy-day displacement experiments, celestial cues often appeared to bees in the new site, contradicting the stored information on which they had been basing their dances. Although most bees quickly adopted the dance angle reflecting their actual direction of flight relative to the sun, some later reverted to the original dance angle, indicating that the information on which it was based had remained in memory when the new information was being expressed; other bees performed bimodal dances which expressed both sets of information in alternate waggle runs. The separation in memory implied by these behaviors may reflect a neural strategy for updating a previously stored relationship between celestial and terrestrial references with new information presented by seasonal changes in the sun's course or by newly learned landmarks.     

Grooming and pollen manipulation in bees (Apoidea): the nature and evolution of movements involving the foreleg

Three modes of self cleaning occur in insects: nibbling by the maxillae, scraping one structure by another in one direction only, and rubbing back and forth while the respective parts are in continuous contact. This paper describes a comprehensive and comparative account of this behaviour in bees, with special reference to the cleaning of or by the forelegs. Bees, like all Hymenoptera, clean various parts of the head, including the mouthparts and the antennae, with the forelegs. Lower Hymenoptera scrape each antenna with either foreleg; in the species of Aculeata that possess the antenna cleaner (strigil) on the foreleg, only the ipsilateral leg is used. The thoracic dorsum of most bees, as in many sphecoid wasps, is scraped in a forward direction by the middle leg; Triepeolus spp., however, use the hind leg, and the Anthophorinae the foreleg. Some beetles and lacewings clean their forelegs in the mouthparts by nibbling and scraping. Most higher Hymenoptera as a rule scrape the foreleg between the ipsilateral maxilla and the labium; bees, however, clamp the foreleg between the flexed ipsilateral middle leg and then scrape it. An evolution of this behaviour is postulated via several intermediate forms derived from original stepping movements. Halictidae and Andrenidae clamp the foreleg for scraping underneath the middle tibia, whereas all other bees nearly always clamp it underneath the middle basitarsus. Very similar movements are used in various species for transferring pollen, oil, or nest materials from the foreleg to the middle leg. It is argued that the original way of pollen carrying in bees must have been by filling the crop through direct eating or by scraping pollen off the foreleg between the ipsilateral maxilla and the labium. The latter movement is widespread among bees and is homologous to the normal foreleg cleaning in the mouthparts of most other Hymenoptera. The efficiency of this behaviour is enhanced in many lower bees by a comb on the galea, which is the homologue of a similar structure widespread among aculeate wasps. In higher bees, Apidae and Anthophoridae, the galeal comb is replaced by an equifunctional stipes comb. Many bees have neither of these types of maxillary combs.     

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.     

Honey bees store landmarks in an egocentric frame of reference

Honey bees are well known to rely on stored landmark information to locate a previously visited site. While various mechanisms underlying insect navigation have been thoroughly explored, little is yet known about the degree of integration of spatial parameters to form higher-level spatial representations. In this paper we explore the basic interactions between landmark cues and directional cues, which stand at the basis of our understanding of piloting mechanisms. A novel experimental paradigm allowed us independent manipulation of each parameter in a highly controlled environment. The approach taken was twofold: cue-conflict experiments were first conducted to examine the interactions between positional cues and directional cues. The bees were then successively deprived of sensory cues to question the dependence of landmark navigation on context cues. Our results confirm previous findings that landmark cues are used in concert with external directional cues if present. Conversely, the bees' ability to locate a food site was not disrupted in the absence of an external directional reference. Thus, bees store landmark memories in an egocentric frame of reference and only loose and facultative associations between visual memories and compass cues are formed.