Influence of flight time and flight environment on distance communication by dancing honey bees

Forager honey bees communicate the distance of food sources to nest mates through waggle dances, but how do bees measure these distances? Recent work suggests that bees measure distance flown in terms of the extent of image motion (integrated optic flow) that is experienced during flight. However, it is known that optic flow also regulates the speed of flight. Therefore, the duration of the flight to a destination is likely to co-vary with the optic flow that is experienced en route. This makes it difficult to tease apart the potential roles of flight duration and optic flow as cues in estimating distance flown. Here we examine whether flight duration alone can serve as an indicator of distance. We trained bees to visit feeders at two sites located in optically different environments, but positioned such that the flight durations to the two sites were similar. The distance estimates for the two sites, as reported in the waggle dance, were compared. We found that dances differed significantly between the two sites, even though flight times were similar. Flight time perse was a poor predictor of waggle dance behaviour. We conclude that foraging bees do not simply signal flight time as their measure of distance in the waggle dance; the environment through which they fly plays a dominant role. Received 11 April 2005; revised 16 May 2005; accepted 3 June 2005.     

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.     

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.     

Interaction between Varroa destructor and imidacloprid reduces flight capacity of honeybees

Current high losses of honeybees seriously threaten crop pollination. Whereas parasite exposure is acknowledged as an important cause of these losses, the role of insecticides is controversial. Parasites and neonicotinoid insecticides reduce homing success of foragers (e.g. by reduced orientation), but it is unknown whether they negatively affect flight capacity. We investigated how exposing colonies to the parasitic mite Varroa destructor and the neonicotinoid insecticide imidacloprid affect flight capacity of foragers. Flight distance, time and speed of foragers were measured in flight mills to assess the relative and interactive effects of high V. destructor load and a field-realistic, chronic sub-lethal dose of imidacloprid. Foragers from colonies exposed to high levels of V. destructor flew shorter distances, with a larger effect when also exposed to imidacloprid. Bee body mass partly explained our results as bees were heavier when exposed to these stressors, possibly due to an earlier onset of foraging. Our findings contribute to understanding of interacting stressors that can explain colony losses. Reduced flight capacity decreases the food-collecting ability of honeybees and may hamper the use of precocious foraging as a coping mechanism during colony (nutritional) stress. Ineffective coping mechanisms may lead to destructive cascading effects and subsequent colony collapse.     

Honeybees prefer warmer nectar and less viscous nectar,regardless of sugar concentration

The internal temperature of flowers may be higher than air temperature, and warmer nectar could offer energetic advantages for honeybee thermoregulation, as well as being easier to drink owing to its lower viscosity. We investigated the responses of Apis mellifera scutellata (10 colonies) to warmed 10% w/w sucrose solutions, maintained at 20–35°C, independent of low air temperatures, and to 20% w/w sucrose solutions with the viscosity increased by the addition of the inert polysaccharide Tylose (up to the equivalent of 34.5% sucrose). Honeybee crop loads increased with nectar temperature, as did the total consumption of sucrose solutions over 2 h by all bees visiting the feeders. In addition, the preference of marked honeybees shifted towards higher nectar temperatures with successive feeder visits. Crop loads were inversely proportional to the viscosity of the artificial nectar, as was the total consumption of sucrose solutions over 2 h. Marked honeybees avoided higher nectar viscosities with successive feeder visits. Bees thus showed strong preferences for both warmer and less viscous nectar, independent of changes in its sugar concentration. Bees may benefit from foraging on nectars that are warmer than air temperature for two reasons that are not mutually exclusive: reduced thermoregulatory costs and faster ingestion times due to the lower viscosity.     

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.     

Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers

Parasites by drawing nutrition from their hosts can exert an energetic stress on them. Honeybee foragers with their high metabolic demand due to flight are especially prone to such a stress when they are infected. We hypothesized that infection by the microsporidian gut parasite Nosema ceranae can lower the hemolymph sugar level of an individual forager and uncouple its energetic state from its normally tight correlation with the colony energetic state. We support our hypothesis by showing that free-flying foragers that are infected have lower trehalose levels than uninfected ones but the two do not differ in their trehalose levels when fed until satiation. The trehalose level of infected bees was also found to decline at a faster rate while their glucose level is maintained at a quantity comparable to uninfected bees. These results suggest that infected foragers have lower flying ability and the intriguing possibility that the carbohydrate levels of an individual bee can act as a modulator of its foraging behavior, independent of social cues such as colony demand for nectar. We discuss the importance of such pathophysiological changes on foraging behavior in the context of the recently observed colony collapses.     

Influence of visual targets and landmarks on honey bee foraging and waggle dancing

Animals use diverse sensory stimuli to navigate their environment and to recognize rewarding food sources.Honey bees use visual atributes of the targeted food source,such as its color,shape,size,direction and distance from the hive,and the landmarks around it to navigate during foraging.They transmit the location information of the food source to other bees if it is highly rewarding.To investigate the relative importance of these attributes,we trained bees to feeders in two different experiments.In the first experiment,we asked whether bees prefer to land on(a)a similar feeder at a different distance on the same heading or on(b)a visually distinct feeder located at the exact same location.We found that,within a short foraging range,bees relied heavily on the color and the shape of the food source and to a lesser extent on its distance from the hive.In the second experiment,we asked if moving the main landmark or the feeder(visual target)influenced recruitment dancing for the feeder.We found that foragers took longer to land and danced fewer circuits when the location of the food source,or a major landmark associated with it,changed.These results demonstrate that prominent visual atributes of food sources and landmarks are evidently more reliable than distance information and that foraging bees heavily utilize these visual cues at the later stages of their journey.     

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.     

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.     

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.     

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.     

Effects of recent experience on foraging decisions by bumble bees

The temporal and spatial scales employed by foraging bees in sampling their environment and making foraging decisions should depend both on the limits of bumble bee memory and on the spatial and temporal pattern of rewards in the habitat. We analyzed data from previous experiments to determine how recent foraging experience by bumble bees affects their flight distances to subsequent flowers. A single visit to a flower as sufficient to affect the flight distance to the next flower. However, longer sequences of two or three visits had an additional effect on the subsequent flight distance of individual foragers. This suggests that bumble bees can integrate information from at least three flowers for making a subsequent foraging decision. The existence of memory for floral characteristics at least at this scale may have significance for floral selection in natural environments.     

Juvenile hormone levels in honey bee (Apis mellifera L.) foragers: foraging experience and diurnal variation

A rising blood titer of juvenile hormone (JH) in adult worker honey bees is associated with the shift from working in the hive to foraging. We determined whether the JH increase occurs in anticipation of foraging or whether it is a result of actual foraging experience and/or diurnal changes in exposure to sunlight. We recorded all foraging flights of tagged bees observed at a feeder in a large outdoor flight cage. We measured JH from bees that had taken 1, 3-5, or >100 foraging flights and foragers of indeterminate experience leaving or entering the hive. To study diurnal variation in JH, we sampled foragers every 6h over one day. Titers of JH in foragers were high relative to nurses as in previous studies, suggesting that conditions in the flight cage had no effect on the relationship between foraging behavior and JH. Titers of JH in foragers showed no significant effects of foraging experience, but did show significant diurnal variation. Our results indicate that the high titer of JH in foragers anticipates the onset of foraging and is not affected by foraging experience, but is modulated diurnally.     

The effect of optic flow cues on honeybee flight control in wind

To minimize the risk of colliding with the ground or other obstacles, flying animals need to control both their ground speed and ground height. This task is particularly challenging in wind, where head winds require an animal to increase its airspeed to maintain a constant ground speed and tail winds may generate negative airspeeds, rendering flight more difficult to control. In this study, we investigate how head and tail winds affect flight control in the honeybee Apis mellifera, which is known to rely on the pattern of visual motion generated across the eye—known as optic flow—to maintain constant ground speeds and heights. We find that, when provided with both longitudinal and transverse optic flow cues (in or perpendicular to the direction of flight, respectively), honeybees maintain a constant ground speed but fly lower in head winds and higher in tail winds, a response that is also observed when longitudinal optic flow cues are minimized. When the transverse component of optic flow is minimized, or when all optic flow cues are minimized, the effect of wind on ground height is abolished. We propose that the regular sidewards oscillations that the bees make as they fly may be used to extract information about the distance to the ground, independently of the longitudinal optic flow that they use for ground speed control. This computationally simple strategy could have potential uses in the development of lightweight and robust systems for guiding autonomous flying vehicles in natural environments.     

Object Recognition in Flight: How Do Bees Distinguish between 3D Shapes?

Honeybees (Apis mellifera) discriminate multiple object features such as colour, pattern and 2D shape, but it remains unknown whether and how bees recover three-dimensional shape. Here we show that bees can recognize objects by their three-dimensional form, whereby they employ an active strategy to uncover the depth profiles. We trained individual, free flying honeybees to collect sugar water from small three-dimensional objects made of styrofoam (sphere, cylinder, cuboids) or folded paper (convex, concave, planar) and found that bees can easily discriminate between these stimuli. We also tested possible strategies employed by the bees to uncover the depth profiles. For the card stimuli, we excluded overall shape and pictorial features (shading, texture gradients) as cues for discrimination. Lacking sufficient stereo vision, bees are known to use speed gradients in optic flow to detect edges; could the bees apply this strategy also to recover the fine details of a surface depth profile? Analysing the bees’ flight tracks in front of the stimuli revealed specific combinations of flight maneuvers (lateral translations in combination with yaw rotations), which are particularly suitable to extract depth cues from motion parallax. We modelled the generated optic flow and found characteristic patterns of angular displacement corresponding to the depth profiles of our stimuli: optic flow patterns from pure translations successfully recovered depth relations from the magnitude of angular displacements, additional rotation provided robust depth information based on the direction of the displacements; thus, the bees flight maneuvers may reflect an optimized visuo-motor strategy to extract depth structure from motion signals. The robustness and simplicity of this strategy offers an efficient solution for 3D-object-recognition without stereo vision, and could be employed by other flying insects, or mobile robots.     

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.     

Monitoring Flower Visitation Networks and Interactions between Pairs of Bumble Bees in a Large Outdoor Flight Cage

Pollinators, such as bees, often develop multi-location routes (traplines) to exploit subsets of flower patches within larger plant populations. How individuals establish such foraging areas in the presence of other foragers is poorly explored. Here we investigated the foraging patterns of pairs of bumble bees (Bombus terrestris) released sequentially into an 880m² outdoor flight cage containing 10 feeding stations (artificial flowers). Using motion-sensitive video cameras mounted on flowers, we mapped the flower visitation networks of both foragers, quantified their interactions and compared their foraging success over an entire day. Overall, bees that were released first (residents) travelled 37% faster and collected 77% more nectar, thereby reaching a net energy intake rate 64% higher than bees released second (newcomers). However, this prior-experience advantage decreased as newcomers became familiar with the spatial configuration of the flower array. When both bees visited the same flower simultaneously, the most frequent outcome was for the resident to evict the newcomer. On the rare occasions when newcomers evicted residents, the two bees increased their frequency of return visits to that flower. These competitive interactions led to a significant (if only partial) spatial overlap between the foraging patterns of pairs of bees. While newcomers may initially use social cues (such as olfactory footprints) to exploit flowers used by residents, either because such cues indicate higher rewards and/or safety from predation, residents may attempt to preserve their monopoly over familiar resources through exploitation and interference. We discuss how these interactions may favour spatial partitioning, thereby maximising the foraging efficiency of individuals and colonies.     

Foraging costs in bumblebees: field conditions cause large individual differences

Summary: Here, we present results from two foraging studies with the bumblebee Bombus terrestris L. We used the doubly labelled water technique which makes it possible to estimate energetic costs of free flight in a natural environment. One study was carried out in windy weather in the open, the second in a large greenhouse under controlled conditions. Individual mass-specific metabolic rates from the open-air study varied widely (159.5 to 750.2 W kg^-1; n = 7) and differed significantly from expected values predicted from laboratory data. Results from the greenhouse study were closer to expectations and the range of individual metabolic rates was much narrower (405.0 to 485.5 W kg^-1; n = 8). The range of field metabolic rates was three to four times larger than that of laboratory studies (Heinrich, 1975; Ellington et al., 1990; Cooper, 1993), which might reflect the fact that only a relatively small percentage (25 - 30 %) of bees are 'co-operative' in laboratory flight cost measurements (Hanauer-Thieser and Nachtigall, 1995; C.P. Ellington and T.J. Wolf, pers. observations). However, all bees flew in the field studies, even in strong winds. We conclude that estimates of energetic costs of free flight using laboratory data (time/activity/laboratory = TAL), an approach regularly used in tests of foraging models, might not be appropriate under many natural conditions. Whereas the TAL method provided a good estimate of mean metabolic rate it is a poor method for studies in which individual variations are of interest.     

Bees do not use nearest-neighbour rules for optimization of multi-location routes

Animals collecting patchily distributed resources are faced with complex multi-location routing problems. Rather than comparing all possible routes, they often find reasonably short solutions by simply moving to the nearest unvisited resources when foraging. Here, we report the travel optimization performance of bumble-bees (Bombus terrestris) foraging in a flight cage containing six artificial flowers arranged such that movements between nearest-neighbour locations would lead to a long suboptimal route. After extensive training (80 foraging bouts and at least 640 flower visits), bees reduced their flight distances and prioritized shortest possible routes, while almost never following nearest-neighbour solutions. We discuss possible strategies used during the establishment of stable multi-location routes (or traplines), and how these could allow bees and other animals to solve complex routing problems through experience, without necessarily requiring a sophisticated cognitive representation of space.