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.     

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.     

Persistence to Unrewarding Feeding Locations by Honeybee Foragers (Apis mellifera): the Effects of Experience,Resource Profitability and Season

Honeybee foragers that find a profitable food source quickly establish spatiotemporal memories, which allow them to return to this foraging site on subsequent days. The aim of this study was to investigate how the previous experience of honeybee foragers at a feeding location affects their persistence at that location once food is no longer available. We hypothesised that persistence would be greater to locations that were more rewarding (closer to the hive, higher concentration of sucrose solution), for which a bee had greater prior experience (0.5‐h vs. 2‐h training access), and at times of the year of lower nectar availability in the environment. We studied individually marked worker bees from four colonies trained to sucrose‐solution feeders. Our results support most of these predictions. Persistence, measured both in duration and number of visits, was greater to locations that previously offered sucrose solution of higher concentration (2 m vs. 1 m ) or were closer to the hive (20 m vs. 450 m). Persistence was also greater in bees that had longer access at the feeder before the syrup was terminated (2 h vs. 0.5 h). However, contrary to our prediction, persistence was not higher in the season of the lowest nectar availability in the environment in the study year. In summary, honeybees show considerable persistence at foraging sites that ceased providing rewards. The decision to abandon a foraging site depends on the profitability the forager experienced when the foraging site was still rewarding.     

Going with the flow: a brief history of the study of the honeybee’s navigational ‘odometer’

Honeybees navigate to a food source using a sky-based compass to determine their travel direction, and an odometer to register how far they have travelled. The past 20 years have seen a renewed interest in understanding the nature of the odometer. Early work, pioneered by von Frisch and colleagues, hypothesized that travel distance is measured in terms of the energy that is consumed during the journey. More recent studies suggest that visual cues play a role as well. Specifically, bees appear to gauge travel distance by sensing the extent to which the image of the environment moves in the eye during the journey from the hive to the food source. Most of the evidence indicates that travel distance is measured during the outbound journey. Accumulation of odometric errors is restricted by resetting the odometer every time a prominent landmark is passed. When making detours around large obstacles, the odometer registers the total distance of the path that is flown to the destination, and not the “bee-line” distance. Finally, recent studies are revealing that bees can perform odometry in three dimensions.     

Effect of Foraging Distance on the Thermal Behaviour of Honeybees during Dancing,Walking and Trophallaxis

By means of infrared thermography and without disturbing social interactions, the correlation between thoracic temperature in honeybees, Apis mellifera carnica, upon their return to the hive and their foraging distance was investigated. Thoracic temperature while dancing and walking and during trophallactic contact with hive bees decreased with increasing flight distance. In bees foraging 0.5, 1, 1.5 and 2 molar sucrose solutions from a distance of 120 m, dancing temperature amounted to 38.4, 40.1, 40.9 and 40.6 °C, respectively; while in bees foraging from a distance of 2950 m it amounted to 36.6, 38.4, 38.6 and 39.1 °C, respectively. The rate of decrease in dancing temperature per 1000 m increase in flight distance was 0.64, 0.47, 0.81 and 0.54 °C with a 0.5, 1, 1.5 and 2 molar sucrose solution, respectively. Both at short and at long flight distances, the relationship between thoracic temperature and sucrose concentration of the food followed a non-linear curve, which flattened at concentrations higher than 1 mol/1. The experiments showed that inside the hive the foragers' level of thermoregulation depends not only on the energy (sugar) content of the food; but rather, the level of thermoregulation corresponds to the general quality of the food source, which includes both energy content and distance from the hive. Because the thermal behaviour of foragers correlates with several behavioural parameters indicating the bees' foraging tendency and their eagerness to dance, thoracic temperature seems to be a correlate of the profitability of foraging.     

Foraging navigation of hornets studied in natural habitats and laboratory experiments

Foraging flights have been studied in three species of hornets (Vespa mandarinia, V. simillima and V. analis) in the field and the laboratory. Hornets seem to use multiple navigational cues for visiting a familiar feeding place. They could orient towards the feeding place immediately after they rose in air from the nest without directly viewing the feeder. They could visit the feeding place after dark at a luminosity 8 lux. These data suggest that they can navigate for some distance with few external cues. Hornets also seem to rely on visual cues for their mid-range navigation. They used some structures on their way as navigational landmarks to negotiate. Individual hornets are supposed to have their own landmarks. Olfactory cues seem to be used to find a new feeding place or to recruit other member. In the approach flight hornets seemed to use multiple visual cues such as the visual characteristics of the feeder and the wider scenery around the feeder. Even if the feeder in training was removed during the test, they flew with a smooth course as if they were pin-pointing the missing feeder, but without sitting on the ground. Hornets learnt how to fly to reach the feeder without external cues after passing by the last visual landmark under conditions with extremely poor visual cues. The present work suggests that hornets retain multiple navigational cues during repeated foraging behavior, and which cues they use seems to depend upon environmental conditions.     

The Shaking Signal of the Honey Bee Informs Workers to Prepare for Greater Activity

One of the most conspicuous activities of worker bees inside a hive is the shaking of other workers. This shaking has long been suspected to be a communication behavior, but its information content and function have until recently remained mysterious. Prior studies of the colony-level patterns of the production of the shaking signal suggest strongly that this signal serves to arouse workers to greater activity, such as at times of good foraging. Data from our observations of individual bees bolster the hypothesis that the shaking signal informs workers to prepare for a higher level of activity. We followed foragers in a colony whose only source of ‘nectar’ was a sugar-water feeder and discovered that when the feeder was left empty for 1–3 d and then refilled, the first bees to find the food initially produced only shaking signals upon return to the hive. It was not until they had completed several trips to the feeder that they began to produce waggle dances. Evidently, the shaking signal and the waggle dance function together to stimulate a colony's foragers to activity.     

Bumble bee olfactory information flow and contact-based foraging activation

Nestmate foraging activation and interspecific variation in foraging activation is poorly understood in bumble bees, as compared to honey bees and stingless bees. We therefore investigated olfactory information flow and foraging activation in the New World bumble bee species, Bombus impatiens. We (1) tested the ability of foragers to associate forager-deposited odor marks with rewarding food, (2) determined whether potential foragers will seek out the food odor brought back by a successful forager, and (3) examined the role of intranidal tactile contacts in foraging activation. Bees learned to associate forager-deposited odor marks with rewarding food. They were significantly more attracted to an empty previously rewarding feeder presented at a random position within an array of eight previously non-rewarding feeders. However, foragers did not exhibit overall odor specificity for short-term, daily floral shifts. For two out of three tested scents, activated foragers did not significantly prefer the feeder providing the same scent as that brought back by a successful forager. Finally, bees contacted by the successful forager inside the nest were significantly more likely to leave the nest to forage (38.6% increase in attempts to feed from empty feeders) than were non-contacted bees. This is the first demonstration that tactile contact, a hypothesized evolutionary basal communication mechanism in the social corbiculate bees, is involved in bumble bee foraging activation. Received 4 September 2007; revised 30 May 2008; accepted 15 July 2008.     

Olfactory learning in the stingless bee Tetragonisca angustula (Hymenoptera, Apidae, Meliponini)

Tetragonisca angustula stingless bees are considered as solitary foragers that lack specific communication strategies. In their orientation towards a food source, these social bees use chemical cues left by co-specifics and the information obtained in previous foraging trips by the association of visual stimuli with the food reward. Here, we investigated their ability to learn the association between odors and reward (sugar solution) and the effect on learning of previous encounters with scented food either inside the hive or during foraging. During food choice experiments, when the odor associated with the food was encountered at the feeding site, the bees’ choice is biased to the same odor afterwards. The same was not the case when scented food was placed inside the nest. We also performed a differential olfactory conditioning of proboscis extension response with this species for the first time. Inexperienced bees did not show significant discrimination levels. However, when they had had already interacted with scented food inside the hive, they were able to learn the association with a specific odor. Possible olfactory information circulation inside the hive and its use in their foraging strategies is discussed.     

Optic flow informs distance but not profitability for honeybees

How do flying insects monitor foraging efficiency? Honeybees (Apis mellifera) use optic flow information as an odometer to estimate distance travelled, but here we tested whether optic flow informs estimation of foraging costs also. Bees were trained to feeders in flight tunnels such that bees experienced the greatest optic flow en route to the feeder closest to the hive. Analyses of dance communication showed that, as expected, bees indicated the close feeder as being further, but they also indicated this feeder as the more profitable, and preferentially visited this feeder when given a choice. We show that honeybee estimates of foraging cost are not reliant on optic flow information. Rather, bees can assess distance and profitability independently and signal these aspects as separate elements of their dances. The optic flow signal is sensitive to the nature of the environment travelled by the bee, and is therefore not a good index of flight energetic costs, but it provides a good indication of distance travelled for purpose of navigation and communication, as long as the dancer and recruit travel similar routes. This study suggests an adaptive dual processing system in honeybees for communicating and navigating distance flown and for evaluating its energetic costs.     

Recruitment of honeybees to non-scented food sources

Small groups of honeybees (five to nine individuals) were trained to forage at feeders 150 m, 300 m and 800 m from an observation hive. Their behaviour in the hive and at the feeder was recorded by observers that maintained continuous radio contact with one another. At low concentrations of sugar in the feeder (0.5 mol x l(-1)) foragers do not dance in the hives, their flights to the feeder are often undertaken alone, they land immediately after arrival at the site and no recruits from the hive landed on the feeder during 30 h of observation. Raising the concentration of sugar in the feeder to 2 mol x l(-1) leads to vigorous dancing by the foragers and the gradual (over 10-15 min) synchronisation of their flights so that they arrive in groups of up to five bees at the feeder and undertake circular "buzzing" flights before landing. Such behaviour of the foragers is associated with the appearance of recruits which were never seen to fly around the feeder and land alone or before the foragers. Recruits typically circle the feeder together with foragers and land with them or continue their circling flights to land about 10 s later. While circling the feeder recruits, but not foragers, will fly after a moving lure if the presentation of the lure is accompanied by the release of geraniol scent. We propose that recruits that have witnessed a waggle dance are unlikely to find a non-scented feeder unless the foragers continue their flights to that feeder and provide supplementary visual and/or olfactory cues, at least in the vicinity of the feeder. We propose that the synchronisation of the flights of foragers and their behaviour at the feeding site is a strategy designed to overcome a navigational gap in the recruiting process in which the dance can indicate the general area of a food source but not the precise position of a highly localised site.     

Do foraging bumblebees scent-mark food sources and does it matter?

Summary The foraging of worker bees of Bombus terrestris visiting artificial feeders in a climatic test chamber was investigated. The behaviour of worker bees visiting rewarding and unrewarding feeders is completely different. Of all flower visits to rewarding feeders 94% are probing-visits, i.e. the bees land on the flower and probe for nectar. In contrast, only 0.3% of all visits to unrewarding feeders are probing-visits, whereas 47% are approach-visits, i.e., the bees approach the feeders without landing. Exchanging feeder discs proves that the signal used for discrimination must be associated with the plastic disc used as landing platform. Most probably it involves scent-marking of the rewarding feeders with components of high and low volatility. The mean foraging efficiency of bees in a scent-marked foraging arena is 5.7 mg sugar/min and drops to 2.8 mg sugar/min after the scent marked discs are replaced by clean ones. Three components generate this drop in foraging efficiency: (1) the between-flower flight time increases, i.e. the bees search for a longer time before landing on flowers, (2) the bees no longer discriminate between rewarding and unrewarding feeders, and (3) the bees probe empty feeders longer than necessary; obviously they expect to find nectar.     

Location and Color Learning in Bumblebees in a Two-Phase Conditioning Experiment

Bees use spatial and visual cues that characterize flowers to make dietary choices. If two such cues always appear together nonambiguously, they provide identical information. In such cases, do bees base dietary choices on one cue and ignore the other, or do they consider both cues? We allowed bumblebees to forage on two patches of artificial flowers that differed in location, color, and reward presence in a two-phase experiment. We switched either the display color, the location, or both the color and the location associated with the rewarding patch between phases. We tested for the effects of the switch on the bees' choices. Immediately following a switch in the location or both the location and the color of the rewarding patch, the bees' performance decreased, as they continued to visit the patch that was previously rewarding. This decrease did not occur when only the color of the rewarding patch was changed or in no-change controls. We suggest that the bees' foraging choices were guided mostly by a location cue when both the location and the color conveyed the same information.     

Complex memories in honeybees: can there be more than two?

Foraging honeybees are likely to learn visual and chemical cues associated with many different food sources. Here, we explore how many such sources can be memorized and recalled. Marked bees were trained to visit two (or three) sugar feeders, each placed at a different outdoor location and carrying a different scent. We then tested the ability of the bees to recall these locations and fly to them, when the training scents were blown into the hive, and the scents and food at the feeders were removed. When trained on two feeder locations, each associated with a different scent, the bees could correctly recall the location associated with each scent. However, this ability broke down when the number of scents and feeder locations was increased to three. Performance was partially restored when each of the three training feeders was endowed with an additional cue, namely, a distinct colour. Our results suggest that bees can recall a maximum of two locations when each is associated with a different scent. However, this number can be increased if the scent cues are augmented by visual cues. These findings have implications for the ways in which associations are established and laid down in honeybee memory.     

Trophallaxis in the honeybee Apis mellifera (L.): the interaction between flow of solution and sucrose concentration of the exploited food sources

Forager bees arriving at the hive after visiting a nectar source, unload the collected liquid food to recipient hivemates through mouth-to-mouth contact (trophallaxis). We analysed whether the main characteristics that define nectar in energetic terms, that is, rate of production (flow of solution), sucrose concentration and rate of sucrose production (sucrose flow) influence trophallactic behaviour. Individual bees trained to feed at a regulated-flow feeder offering sucrose solution were captured once the foraging visit was complete and placed in an acrylic arena with a recipient bee that had not been fed. The rate at which liquid was transferred during the subsequent trophallactic contact (transfer rate) was analysed as a function of the different solution flows and sucrose concentrations offered at the feeder. A relationship was found between transfer rate during trophallaxis and the flow of solution previously presented at the feeder. This relationship was independent of sucrose concentration when above a certain threshold value (ca. 22% weight on weight). We also analysed whether the rate of sucrose deliverance of the food source (sucrose flow) influenced the rate at which the solution was transferred. No clear relationship was found between the rate of sucrose deliverance during trophallactic events (sucrose transfer rate) and the sucrose flow presented at the feeder. The possibility that trophallaxis could be a communication channel through which quantitative information on food source profitability is transmitted among hivemates is discussed. Copyright 2000 The Association for the Study of Animal Behaviour.     

Route and landmark learning by rats searching for food

Many foraging animals rely on visual landmarks and/or habitual paths to locate important resources. We examined the degree to which rats rely on these cues when they predicted conflicting food locations. In this foraging task, rats were required to find food which could be located using either a fixed route or a nearby visual landmark. In tests, we found that their subsequent search-based estimates of the food location were the same when animals had acquired a long-term memory of the route, the landmark, or both. We show that the degree to which animals rely on the cues depends not only on the discrepancy between the two cues, but also on whether animals can match the testing “view” with a learned “view” that has been acquired during training.     

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.     

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.     

Ants adjust their pheromone deposition to a changing environment and their probability of making errors

Animals must contend with an ever-changing environment. Social animals, especially eusocial insects such as ants and bees, rely heavily on communication for their success. However, in a changing environment, communicated information can become rapidly outdated. This is a particular problem for pheromone trail using ants, as once deposited pheromones cannot be removed. Here, we study the response of ant foragers to an environmental change. Ants were trained to one feeder location, and the feeder was then moved to a different location. We found that ants responded to an environmental change by strongly upregulating pheromone deposition immediately after experiencing the change. This may help maintain the colony''s foraging flexibility, and allow multiple food locations to be exploited simultaneously. Our treatment also caused uncertainty in the foragers, by making their memories less reliable. Ants which had made an error but eventually found the food source upregulated pheromone deposition when returning to the nest. Intriguingly, ants on their way towards the food source downregulated pheromone deposition if they were going to make an error. This may suggest that individual ants can measure the reliability of their own memories and respond appropriately.     

Foragers of the stingless bee Plebeia droryana inform nestmates about the direction,but not the distance to food sources

1. The tropical stingless bees have evolved intricate communication systems to recruit nestmates to food locations. Some species are able to accurately communicate the location of food, whereas others simply announce the presence of food in the environment.
2. Plebeia droryana is a tiny Neotropical stingless bee that, until recently, was thought to use a solitary foraging strategy, that is without the use of a recruitment communication system. However, recent research has indicated that P. droryana might be able to recruit nestmates to specific food source locations.
3. We tested this by studying whether foragers can guide nestmates in the direction and the distance of artificial feeders placed in the vicinity of the colony. We trained bees to a scented sucrose solution feeder at 10 m and placed different feeders either in different directions (experiment 1) or in different distances (experiment 2). We found that P. droryana directs newcomers in the right direction, but distance information does not seem to be communicated.
4. Moreover, we then tested whether newcomers use chemical and visual cues originating from nestmates foraging at the food source, but found no evidence for the use of these social cues provided by conspecifics.
5. The potential mechanism that P. droryana may use to orient recruits toward the food source, however, remains unknown and requires further study.