Honeybee navigation: critically examining the role of the polarization compass

Although it is widely accepted that honeybees use the polarized-light pattern of the sky as a compass for navigation, there is little direct evidence that this information is actually sensed during flight. Here, we ask whether flying bees can obtain compass cues derived purely from polarized light, and communicate this information to their nest-mates through the ‘waggle dance’. Bees, from an observation hive with vertically oriented honeycombs, were trained to fly to a food source at the end of a tunnel, which provided overhead illumination that was polarized either parallel to the axis of the tunnel, or perpendicular to it. When the illumination was transversely polarized, bees danced in a predominantly vertical direction with waggles occurring equally frequently in the upward or the downward direction. They were thus using the polarized-light information to signal the two possible directions in which they could have flown in natural outdoor flight: either directly towards the sun, or directly away from it. When the illumination was axially polarized, the bees danced in a predominantly horizontal direction with waggles directed either to the left or the right, indicating that they could have flown in an azimuthal direction that was 90° to the right or to the left of the sun, respectively. When the first half of the tunnel provided axial illumination and the second half transverse illumination, bees danced along all of the four principal diagonal directions, which represent four equally likely locations of the food source based on the polarized-light information that they had acquired during their journey. We conclude that flying bees are capable of obtaining and signalling compass information that is derived purely from polarized light. Furthermore, they deal with the directional ambiguity that is inherent in polarized light by signalling all of the possible locations of the food source in their dances, thus maximizing the chances of recruitment to it.     

Evidence for instantaneous e-vector detection in the honeybee using an associative learning paradigm

Many insects use the polarization pattern of the sky for obtaining compass information during orientation or navigation. E-vector information is collected by a specialized area in the dorsal-most part of the compound eye, the dorsal rim area (DRA). We tested honeybees' capability of learning certain e-vector orientations by using a classical conditioning paradigm with the proboscis extension reflex. When one e-vector orientation (CS+) was associated with sugar water, while another orientation (CS-) was not rewarded, the honeybees could discriminate CS+ from CS-. Bees whose DRA was inactivated by painting did not learn CS+. When ultraviolet (UV) polarized light (350 nm) was used for CS, the bees discriminated CS+ from CS-, but no discrimination was observed in blue (442 nm) or green light (546 nm). Our data indicate that honeybees can learn and discriminate between different e-vector orientations, sensed by the UV receptors of the DRA, suggesting that bees can determine their flight direction from polarized UV skylight during foraging. Fixing the bees' heads during the experiments did not prevent learning, indicating that they use an 'instantaneous' algorithm of e-vector detection; that is, the bees do not need to actively scan the sky with their DRAs ('sequential' method) to determine e-vector orientation.     

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.     

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.     

Pulsed mass recruitment by a stingless bee, Trigona hyalinata

Research on bee communication has focused on the ability of the highly social bees, stingless bees (Hymenoptera, Apidae, Meliponini) and honeybees (Apidae, Apini), to communicate food location to nest-mates. Honeybees can communicate food location through the famous waggle dance. Stingless bees are closely related to honeybees and communicate food location through a variety of different mechanisms, many of which are poorly understood. We show that a stingless bee, Trigona hyalinata, uses a pulsed mass-recruitment system that is highly focused in time and space. Foragers produced an ephemeral, polarized, odour trail consisting of mandibular gland secretions. Surprisingly, the odour trail extended only a short distance away from the food source, instead of providing a complete trail between the nest and the food source (as has been described for other stingless bees). This abbreviated trail may represent an intermediate strategy between full-trail marking, found in some stingless bees, and odour marking of the food alone, found in stingless bees and honeybees.     

Celestial orientation in bees: the use of spectral cues

Summary The spectral cues used in the bee's celestial compass are investigated by presenting bees dancing on a horizontal comb with unpolarized (or polarized) spectral stimuli. Where appropriate, the use of e-vector information is prevented by painting out the specialized dorsal margin of the bee's eye (POL area, Fig. 1). This area has been shown to mediate e-vector information (Fig. 3; Wehner 1982), whereas the remainder of the dorsal retina is sufficient for mediating spectral information (Fig. 4).Spectral cues are used by the bees to discriminate between sun and sky (Fig. 4). According to physical reality (Fig. 2), a long-wavelength stimulus is taken as the sun, whereas a short-wavelength stimulus is expected by the bee to lie anywhere within the antisolar half of the sky (Figs. 5 and 6). This is in accord with the bee's e-vector compass in which e-vectors are confined to the antisolar half of the sky (Fig. 9).In general, spectral cues do not provide precise compass information except when a full celestial colour gradient is available including the solar and the antisolar meridian (Figs. 7 and 8).     

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.     

Interaction of behavioral and autonomic thermoregulation in cold exposed pigeons

Summary When bees dance on a horizontal comb in an enclosed hive, they set the direction of their waggle runs with reference to an artificial light source. If this light contains wavelengths long enough to excite the blue or green receptors in the bee's eye, the dance direction relative to the lamp is the same as it would be relative to the sun. But if the emitted light excites only the UV receptors the bee dances in the opposite direction. Evidently the bee interprets the UV-colored light source as a part of the sky with azimuth opposite to that of the sun.     

The role of skylight polarization in the orientation of a day-migrating bird species

To assess the role of skylight polarization in the orientation system of a day-migrating bird, Yellow-faced Honeyeaters (Lichenostomus chrysops, Meliphagidae) were tested in funnel cages for their directional preferences. In control tests in the natural local geomagnetic field under the clear natural sky, they preferred their normal migratory course. Manipulations of the e-vector by depolarizing the skylight or rotating the axis of polarization failed to affect the orientation as long as the natural geomagnetic field was present. When deprived of magnetic information, the birds continued in their normal migratory direction as long as they had access to information from the natural sky, or when either the sun or polarized light was available. However, when sun was hidden by clouds, depolarizers caused disorientation. — These findings indicate that polarized skylight can be used for orientation when no other known cues are available. However in the hierarchy of cues of this species, the polarization pattern clearly ranks lower than information from the geomagnetic field.     

The waggle dance of the honey bee: Which bees following a dancer successfully acquire the information?

During the waggle dance of the honeybee, the dancer is able to tell her nestmates the distance and direction to a rich food source (Frisch, 1967). Little is known about how waggle dance followers are able to read the waggle dance in the darkness of a hive. Initial observations showed that not all of the bees that appear to be dance followers behave the same. Some bees maneuver themselves behind the dancer, while others do not. The paths of a single dancer, trained to an artificial food source, and her followers were traced during the waggle runs. The success of these dance followers was compared to their position relative to the dancer. The results of this study show that during a waggle run a dance follower must position itself within a 30° arc behind the dancer in order to obtain the dance information. The results suggest that bees are using the position of their own bodies to determine direction.     

Social learning of floral odours inside the honeybee hive

A honeybee hive serves as an information centre in which communication among bees allows the colony to exploit the most profitable resources in a continuously changing environment. The best-studied communication behaviour in this context is the waggle dance performed by returning foragers, which encodes information about the distance and direction to the food source. It has been suggested that another information cue, floral scents transferred within the hive, is also important for recruitment to food sources, as bee recruits are more strongly attracted to odours previously brought back by foragers in both honeybees and bumble-bees. These observations suggested that honeybees learn the odour from successful foragers before leaving the hive. However, this has never been shown directly and the mechanisms and properties of the learning process remain obscure. We tested the learning and memory of recruited bees in the laboratory using the proboscis extension response (PER) paradigm, and show that recruits indeed learn the nectar odours brought back by foragers by associative learning and retrieve this memory in the PER paradigm. The associative nature of this learning reveals that information was gained during mouth-to-mouth contacts among bees (trophallaxis). Results further suggest that the information is transferred to long-term memory. Associative learning of food odours in a social context may help recruits to find a particular food source faster.     

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.     

Evidence for the possible existence of a second polarization-vision pathway in the locust brain

For spatial orientation and navigation, many insects derive compass information from the polarization pattern of the blue sky. The desert locust Schistocerca gregaria detects polarized light with a specialized dorsal rim area of its compound eye. In the locust brain, polarized-light signals are passed through the anterior optic tract and tubercle to the central complex which most likely serves as an internal sky compass. Here, we suggest that neurons of a second visual pathway, via the accessory medulla and posterior optic tubercle, also provide polarization information to the central complex. Intracellular recordings show that two types of neuron in this posterior pathway are sensitive to polarized light. One cell type connects the dorsal rim area of the medulla with the medulla and accessory medulla, and a second type connects the bilaterally paired posterior optic tubercles. Given the evidence for a role of the accessory medulla as the master clock controlling circadian changes in behavioral activity in flies and cockroaches, our data open the possibility that time-compensated polarized-light signals may reach the central complex via this pathway for time-compensated sky-compass navigation.     

Transmedulla Neurons in the Sky Compass Network of the Honeybee (Apis mellifera) Are a Possible Site of Circadian Input

Honeybees are known for their ability to use the sun’s azimuth and the sky’s polarization pattern for spatial orientation. Sky compass orientation in bees has been extensively studied at the behavioral level but our knowledge about the underlying neuronal systems and mechanisms is very limited. Electrophysiological studies in other insect species suggest that neurons of the sky compass system integrate information about the polarization pattern of the sky, its chromatic gradient, and the azimuth of the sun. In order to obtain a stable directional signal throughout the day, circadian changes between the sky polarization pattern and the solar azimuth must be compensated. Likewise, the system must be modulated in a context specific way to compensate for changes in intensity, polarization and chromatic properties of light caused by clouds, vegetation and landscape. The goal of this study was to identify neurons of the sky compass pathway in the honeybee brain and to find potential sites of circadian and neuromodulatory input into this pathway. To this end we first traced the sky compass pathway from the polarization-sensitive dorsal rim area of the compound eye via the medulla and the anterior optic tubercle to the lateral complex using dye injections. Neurons forming this pathway strongly resembled neurons of the sky compass pathway in other insect species. Next we combined tracer injections with immunocytochemistry against the circadian neuropeptide pigment dispersing factor and the neuromodulators serotonin, and γ-aminobutyric acid. We identified neurons, connecting the dorsal rim area of the medulla to the anterior optic tubercle, as a possible site of neuromodulation and interaction with the circadian system. These neurons have conspicuous spines in close proximity to pigment dispersing factor-, serotonin-, and GABA-immunoreactive neurons. Our data therefore show for the first time a potential interaction site between the sky compass pathway and the circadian clock.     

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.     

E-Vector orientation in bees

Summary If an insect is able to determine the direction of polarization in any point of the sky, this ability does not in itself guarantee that the insect can orientate unambiguously. Such would only be the case, if every point in the sky had its own exclusive direction of polarization. In thee-vector pattern of the sky, however, each direction of polarization is found at many different points. For compass orientation the insect has therefore to use some information on the geometry of thee-vector pattern in the sky. In general, eache-vector occurs twice at a given elevation (Fig. 1). The angular separation between the positions of identicale-vectors depends on the elevations of thee-vectors above the horizon and on the height of the sun. Except at sunrise and sunset, 180°.If a bee is trained to fly in a certain direction to a food source, the direction of its waggle dance on a horizontal comb points directly towards the goal (provided that the bee is able to view the sky). However, if the bee is only allowed to view a singlee-vector in the sky (or a single artificially adjustede-vector), it should perform ambiguous orientation. One expects the bee to prefer two dance directions separated by the proper angular distance . One of these two dance directions should point at the food source.The bees indeed dance in two directions. However, there are two unexpected results: (1) The angular distance between the two preferred directions invariably amounts to =180°. (2) One of the preferred directions points closely, but not exactly at the goal. What one can deduce from these single-e-vector tests is that the bee uses a rather generalized internal representation of thee-vector pattern in the sky. This paper describes the generale-vector characteristic applied by a dancing bee that only views a singlee-vector in the sky (diameter of the celestial patch or the artificially polarized light source 10°). This generale-vector characteristic of the bee (Fig. 9) more closely fits the meane-vector distribution near the zenith thane-vector distributions in other parts of the sky (Fig. 11).This article is dedicated to Prof. Dr. H. Autrum in honor of his seventieth birthdayThe research has been supported by Swiss National Science Foundation Grant 3.814.72, continued by Grant 3.529.75, and by the Academy of Science and Literature at Mainz. We would like to thank Dr. R. Schinz (Purdue University) for cooperation and fruitful discussions as well as Mrs. V. Güttinger, Mrs. A. Rossel-Jäckle, and Miss A. Blischke for technical assistance.     

Polarized light orientation in honey bees: Is time a component in sampling?

Bees on a horizontal comb can orient their dances by a field of polarized light in the zenith even when the degree of polarization of this light field is modulated from 0 to 100%, at frequencies between 0.05 and 25 Hz, with the direction of polarization and the intensity kept constant. The result suggests that bees use a process of polarized light evaluation which probes simultaneously with three or more differently oriented analyser channels. It would follow that, in this experimental situation, time is not a component of sampling.     

Sticking to their choice – honey bee subfamilies abandon declining food sources at a slow but uniform rate

Abstract. 1. The allocation of honey bee foragers among food patches is a result of decisions made by individual bees that are based on internal and external cues.
2. Decision-making processes are often based on internal thresholds. For example, if the quality of the food source is assessed by a forager as exceeding its internal threshold, the bee will continue foraging on that food source.
3. It is often assumed that all individuals have the same threshold and therefore use the same thresholds in decision-making, but because the honey bee queen mates with 12–30 males, the workers within a colony are genetically heterogeneous. Thus, the thresholds used by individual bees may be genetically variable within a colony.
4. Models of colony-level foraging behaviour of honey bees suggest that the rate of abandoning food sources is a critical parameter affecting foraging success. Moreover, these models show that variance among subfamilies in their abandonment rates may increase the colony's foraging efficiency.
5. Experimental data showing the relationship between the probability of abandoning a food source and its profitability are lacking, as is information on any variation in abandonment rates among subfamilies.
6. Abandonment rates were determined experimentally for four honey bee families for seven different sucrose concentrations. The results showed that abandonment rates appear to be invariant among (sub)families. The importance of forager fidelity to declining food sources is discussed with respect to foraging efficiency in a changing environment.     

Visual reliability and information rate in the retina of a nocturnal bee

Nocturnal animals relying on vision typically have eyes that are optically and morphologically adapted for both increased sensitivity and greater information capacity in dim light. Here, we investigate whether adaptations for increased sensitivity also are found in their photoreceptors by using closely related and fast-flying nocturnal and diurnal bees as model animals. The nocturnal bee Megalopta genalis is capable of foraging and homing by using visually discriminated landmarks at starlight intensities. Megalopta's near relative, Lasioglossum leucozonium, performs these tasks only in bright sunshine. By recording intracellular responses to Gaussian white-noise stimuli, we show that photoreceptors in Megalopta actually code less information at most light levels than those in Lasioglossum. However, as in several other nocturnal arthropods, Megalopta's photoreceptors possess a much greater gain of transduction, indicating that nocturnal photoreceptors trade information capacity for sensitivity. By sacrificing photoreceptor signal-to-noise ratio and information capacity in dim light for an increased gain and, thus, an increased sensitivity, this strategy can benefit nocturnal insects that use neural summation to improve visual reliability at night.     

A specialized dorsal rim area for polarized light detection in the compound eye of the scarab beetle Pachysoma striatum

Many animals have been shown to use the pattern of polarized light in the sky as an optical compass. Specialised photoreceptors are used to analyse this pattern. We here present evidence for an eye design suitable for polarized skylight navigation in the flightless desert scarab Pachysoma striatum. Morphological and electrophysiological studies show that an extensive part of the dorsal eye is equivalent to the dorsal rim area used for polarized light navigation in other insects. A polarization-sensitivity of 12.8 (average) can be recorded from cells sensitive to the ultraviolet spectrum of light. Features commonly known to increase the visual fields of polarization-sensitive photoreceptors, or to decrease their spatial resolution, are not found in the eye of this beetle. We argue that in this insect an optically unspecialised area for polarized light detection allows it not be used exclusively for polarized light navigation.