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.     

Honey bee dance communication: waggle run direction coded in antennal contacts?

The behaviour of 38 honeybee dance followers and the patterns of antennal contact between followers and dancer were monitored during ten waggle runs for a feeding site 1200 m from the hive. The analysis was restricted to waggle runs with a maximum of 5 followers, allowing the followers to choose between different positions around the dancer. At the beginning of the waggle run, followers are rather evenly spaced around the dancer. During the waggle run, the followers tend to accumulate at the rear end of the dancer. At the end of the waggle run, all followers are found in a ±60° arc behind the dancer. The body orientation angles of the followers depend on their position relative to the dancer. The follower bees have intense antennal contact with the dancer. At least one temporal parameter of the contact pattern may inform the followers about their position relative to the dancer, may guide the dance followers to the rear end of the dancer and may allow them to extract information about the location of the food source advertised by the dance. The role of antennal contact for dance communication appears to have been underestimated in previous studies. Accepted: 20 February 1999     

The Brief Piping Signal of the Honey Bee: Begging Call or Stop Signal?

For over 40 yr, investigators have recognized that the brief piping signal plays a role in the foraging operation of a honey bee colony. The function of this signal, however, remains uncertain. The main objective of this study was to determine whether, under normal foraging conditions, bees following waggle dancers produce brief piping signals to beg nectar samples from the dancers. We made observations on waggle dancers and their followers in an undisturbed colony whose foragers gathered nectar and pollen from flowers. We found that waggle dancers do often receive brief piping signals, that the bees producing these signals are generally dance followers, and that these signals increase a waggle dancer's tendency to stop dancing. We also found, however, that the brief piping signal is clearly not a begging call; 0 of 41 waggle dancers that received a piping signal from a dance follower gave a nectar sample to the bee that produced the signal. Our results support the hypothesis that the brief piping signal is a stop signal; it serves to shut off waggle dancing. But why some dance followers pipe the dancer they are following, thereby inhibiting her dancing, remains unclear and warrants further investigation.     

Direct Visual Observation of Wing Movements during the Honey Bee Waggle Dance

Recruitment-related behaviours such as waggle dances enable honey bee foragers to inform their nestmates about the location of important resources. However, it is still not known how the information contained in a dance performed in the darkness of the nest is transferred to followers. Although, there are findings indicating that dancing honey bees produce airborne sounds which may convey the information, there has only been indirect evidence that moving wings are the source of these airborne sounds. In this study, honey bee dances were recorded using a high-speed camera in order to directly observe and precisely measure the frequency of wing beats and abdomen wags of dancers. Dancing bees moved their wings for 40.4% of the duration of a waggle run and for only 8.1% of the duration of a circle run. The episodes of wing movements consisted of one to five wing beats and were separated by intervals of motionless wings. The mean frequency of wing beats was 167.0 Hz and significantly differed depending on the number of wing beats in one episode (p < 0.001) and the position of the wings (p = 0.007). The mean frequency of abdomen wags was 14.6 Hz. The mean number of followers was 7.9 and significantly more of them gathered around the abdomens of dancers than around their heads and thoraxes (p = 0.001). The results of this study support the assumption that moving wings are the source of airborne sounds emitted during honey bee dances.     

What attracts honeybees to a waggle dancer?

In the vicinity of a dancer, a honeybee can become a dance follower after touching the dancer or a dance follower with an antenna. If the attraction occurs without such antennal contact, the strength of the attraction over distance depends on several factors: the kind of dance floor (empty open cells versus capped brood cells); whether dancers and dance followers stand on the same substratum or on separate substrata; the position and direction of the attracted bee relative to the dancer bee; the size of the dance group (the dancer plus follower bees); and the light conditions under which the dance takes place. Dances on open cells are significantly more attractive than dances on sealed cells. Dancers on open cells attracted 90% of all followers from within 27 mm (about five to six cell diameters). Dancers on sealed cells attracted 90% of all followers within 18 mm (about three cell diameters). The majority of bees that were attracted by the dancer were standing laterally to the dancer. Dances illuminated by artificial visible light are significantly more attractive than dances illuminated by infrared light. As a group, “glassplate bees” (bees standing mechanically isolated from the dancer bee) were least attracted. Accepted: 11 August 1998     

The acoustic near field of a dancing honeybee

Summary The acoustic near field close to honeybees performing the wagging dance was investigated with pairs of small, matched microphones placed in various positions around the dancing bees. The dance sounds are produced by the wings, which act as an asymmetrical dipole emitter. Close to the abdomen, the sound pressures in the air spaces above and below the plane of the wings are totally out of phase. A zone of very intense acoustical short-circuiting exists close to the edges of the wings, where pressure gradients of about 1 Pa/mm are observed in the dorso-ventral direction (perpendicular to the plane of the wings). The pressure gradients drive air movements with velocity amplitudes up to about 1 m/s. The pressure gradients are much smaller in directions radially away from the bee and decrease rapidly with increasing distance from the wings. The sound pressure detected by a stationary probe at one side of the bee is strongly modulated at 12–13 Hz as a result of the bee's side-to-side wagging. Surprisingly little sound is found near the dancer's head. The positions of the follower bees reflect the properties of the acoustic field: The follower bees place their antennae in the zone of maximum acoustical short-circuiting where the air particle movements are most intense. These observations suggest 1) how follower bees can avoid mixing up the messages carried by the dance sounds when two or more bees are dancing only a few cm apart and 2) how the followers might extract information about a dancer's spatial orientation from the acoustic near field she produces. The observations also provide clues regarding the nature of the putative sound receivers.Dedicated to Professor Dr. Drs. h.c. mult. H. Autrum on the occasion of his 80th birthday     

Informational conflicts created by the waggle dance

The honeybee (Apis mellifera) waggle dance is one of the most intriguing animal communication signals. A dancing bee communicates the location of a profitable food source and its odour. Followers may often experience situations in which dancers indicate an unfamiliar location but carry the scent of a flower species the followers experienced previously at different locations. Food scents often reactivate bees to resume food collection at previously visited food patches. This double function of the dance creates a conflict between the social vector information and the private navigational information. We investigated which kind of information followers with field experience use in this situation and found that followers usually ignored the spatial information encoded by the waggle dance even if they followed a dance thoroughly (five waggle runs or more). They relied on private information about food source locations instead (in 93% of all cases). Furthermore, foragers preferred to follow dancers carrying food odours they knew from previous field trips, independently of the spatial information encoded in the dance. Surprisingly, neither odour identity nor the location indicated by the dancer was an important factor for the reactivation success of a dance. Our results contrast with the assumption that (i) followers usually try to decode the vector information and (ii) dances indicating an unfamiliar location are of little interest to experienced foragers.     

Does the Earth's Magnetic Field Serve as a Reference for Alignment of the Honeybee Waggle Dance?

The honeybee (Apis mellifera) waggle dance, which is performed inside the hive by forager bees, informs hive mates about a potent food source, and recruits them to its location. It consists of a repeated figure-8 pattern: two oppositely directed turns interspersed by a short straight segment, the “waggle run”. The waggle run consists of a single stride emphasized by lateral waggling motions of the abdomen. Directional information pointing to a food source relative to the sun''s azimuth is encoded in the angle between the waggle run line and a reference line, which is generally thought to be established by gravity. Yet, there is tantalizing evidence that the local (ambient) geomagnetic field (LGMF) could play a role. We tested the effect of the LGMF on the recruitment success of forager bees by placing observation hives inside large Helmholtz coils, and then either reducing the LGMF to 2% or shifting its apparent declination. Neither of these treatments reduced the number of nest mates that waggle dancing forager bees recruited to a feeding station located 200 m north of the hive. These results indicate that the LGMF does not act as the reference for the alignment of waggle-dancing bees.     

Do honey bees encode distance information into the wing vibrations of the waggle dance?

An optical technique detected the wing vibration frequency of worker honey bees in an observation hive during the straight run of the waggle dance. Wing oscillation frequencies were recorded from dancing bees after they had visited a feeding station located from 50 to 1600 m from the hive. The bees vibrated their wings more rapidly after they visited nearby stations than when they foraged at more distant feeding stations. For example, the mean frequency of 315 Hz at 50 m dropped to only 207 Hz at 1600 m. Wing vibration frequency appears to be another factor to be added to the elements in the dance known to indicate the distance bees must fly to food sources. These known elements include the duration of the straight run and the number of wagtail movements in the run.     

The scent of the waggle dance

The waggle dance of honey bee (Apis mellifera L.) foragers communicates to nest mates the location of a profitable food source. We used solid-phase microextraction and gas chromatography coupled with mass spectrometry to show that waggle-dancing bees produce and release two alkanes, tricosane and pentacosane, and two alkenes, Z-(9)-tricosene and Z-(9)-pentacosene, onto their abdomens and into the air. Nondancing foragers returning from the same food source produce these substances in only minute quantities. Injection of the scent significantly affects worker behavior by increasing the number of bees that exit the hive. The results of this study suggest that these compounds are semiochemicals involved in worker recruitment. By showing that honey bee waggle dancers produce and release behaviorally active chemicals, this study reveals a new dimension in the organization of honey bee foraging.     

The effects of season,pretraining, and scent on the efficiency of traps for capturing recruited honey bees (Hymenoptera: Apidae)

A portable trap was designed to capture honey bees recruited to the field by dancers. An infrared phototransistor placed in the entrance tunnel of the trap sensed an incoming bee and turned on a talking clock, which in turn activated a voice-actuated audio tape recorder that recorded the time. We tested the effectiveness of traps for capturing bees recruited by four dancer bees (1) during two seasons when local flower densities differed, (2) with or without a group of bees pretrained to enter traps for food, and (3) when the scent used in traps and at the dancers' feeding station was changed just prior to recruitment trials or was not changed. One trap was put out at each of four distances (50, 100, 150, and 200 m) from the hive, while dancers fed on concentrated sucrose at the feeding station located at 150 m in the same direction. Recruited bees that approached the traps but did not enter were counted by observers. More bees were recruited and captured in traps when the local flora was sparse (fall) than when flowers were abundant (summer), when bees were pretrained versus not pretrained, and when the scent was not changed just prior to recruitment trials versus changed. The distributions of number of bees counted at the four distances at scented recruit stations and trapped were similar only when bees were pretrained and the scent was not changed during recruitment trials. However, the highest proportion of bees trapped in a trial at 150 m (distance to dancers' feeding station) was when bees were pretrained and the scent was changed.     

Dynamic range compression in the honey bee auditory system toward waggle dance sounds

Honey bee foragers use a "waggle dance" to inform nestmates about direction and distance to locations of attractive food. The sound and air flows generated by dancer's wing and abdominal vibrations have been implicated as important cues, but the decoding mechanisms for these dance messages are poorly understood. To understand the neural mechanisms of honey bee dance communication, we analyzed the anatomy of antenna and Johnston's organ (JO) in the pedicel of the antenna, as well as the mechanical and neural response characteristics of antenna and JO to acoustic stimuli, respectively. The honey bee JO consists of about 300-320 scolopidia connected with about 48 cuticular "knobs" around the circumference of the pedicel. Each scolopidium contains bipolar sensory neurons with both type I and II cilia. The mechanical sensitivities of the antennal flagellum are specifically high in response to low but not high intensity stimuli of 265-350 Hz frequencies. The structural characteristics of antenna but not JO neurons seem to be responsible for the non-linear responses of the flagellum in contrast to mosquito and fruit fly. The honey bee flagellum is a sensitive movement detector responding to 20 nm tip displacement, which is comparable to female mosquito. Furthermore, the JO neurons have the ability to preserve both frequency and temporal information of acoustic stimuli including the "waggle dance" sound. Intriguingly, the response of JO neurons was found to be age-dependent, demonstrating that the dance communication is only possible between aged foragers. These results suggest that the matured honey bee antennae and JO neurons are best tuned to detect 250-300 Hz sound generated during "waggle dance" from the distance in a dark hive, and that sufficient responses of the JO neurons are obtained by reducing the mechanical sensitivity of the flagellum in a near-field of dancer. This nonlinear effect brings about dynamic range compression in the honey bee auditory system.     

Abdominal grooming in the cockroach: Development of an adult behavior

Chemical or tactile irritants delivered to the dorsomedial region of the abdomen of the cockroach Periplaneta americana. evoke a complex grooming response. In larvae the response consitsts of extension of all six legs and arching of the abdomen which is rubbed against any solid surface presented. In adults, leg extension and arching are accompanied by side to side wagging of the abdomen and rapid scissoring of the wings.In some decapitated late instar larvae, abdominal wagging behavior can be evoked by chemical or tactile stimulation of the dorso-medial region of the abdomen. The form of the wag is somewhat different in these animals than in the adults, and it occurs at a lower frequency.Neuronal circuitry underlying the rhythmic wagging response of the adult may therefore be laid down or made functional in the mid- to late-larval stages. The wagging behavior is not normally expressed until the final ecdysis.A population of sensory setae is found on the abdomen at all stages of development, and some of these are presumed to trigger the grooming behavior when stimulated. The morphology and distribution of some of the adult receptors differs from some of the larval receptors.All larvae, including those late-instar individuals which show an adult-like response (wagging) have identical receptors on the abdomen in terms of morphology, distribution, and general responsiveness. Thus, no obvious changes in abdominal sensory receptors are correlated with the emergence of the wagging behavior. Anatomical and/or functional changes within the central nervous system are most likely responsible for the emergence of adult wagging behavior.     

Variations of brain biogenic amines in mature honeybees and induction of recruitment behavior

Mature honeybees (Apis mellifera L.) old enough to forage (>3 weeks) were segregated into three activity groups: waggle dancers (active foragers), followers of the dancers (potential recruits) and resting bees (not involved in foraging). Dopamine (DA) pathways in the brain of honeybees seemed to be involved in regulation of forager recruitment. Brain DA and N-β-alanyldopamine (NBAD) levels in the dancers were always higher than in followers, and an increased number of dancers was observed after feeding the colony dihydroxy-phenylalanine (DOPA). Dopamine is hypothesized to modulate the neural activity in the calyx of the mushroom bodies related to recruitment behavior. No consistant effect of octopamine (OA) or serotonin (5HT) on recruitment behavior was observed. Levels of all biogenic amines were strongly effected by season and day-to-day whether changes. Some diurnal changes were also observed.     

Intra-Colonial Variability in the Dance Communication in Honeybees (Apis mellifera)

Honeybees have evolved numerous mechanisms for increasing colony-level foraging efficiency, mainly the combined system of scout-recruit division of labour and recruitment communication. A successful forager performs waggle dances on the surface of the comb where it interacts with nectar receivers and dance followers. A forager uses tremble dance when it experiences difficulty finding a receiver bee to unload food upon return to the hive. A bee colony containing numerous subfamilies may increase its efficiency in dance communication if dances are realized by particular groups of specialized individuals or subfamilies rather than by undifferentiated workers. In this study, we determined the subfamily frequencies of waggle and tremble dancers in a colony headed by a naturally mated queen, where the 17 subfamilies can be identified by microsatellite genetic markers. Our results demonstrate that a genetic component is associated with the dance communication in honeybees. More than half of the waggle dances and the tremble dances were performed by workers from only four subfamilies in each case.     

Working against gravity: horizontal honeybee waggle runs have greater angular scatter than vertical waggle runs

The presence of noise in a communication system may be adaptive or may reflect unavoidable constraints. One communication system where these alternatives are debated is the honeybee (Apis mellifera) waggle dance. Successful foragers communicate resource locations to nest-mates by a dance comprising repeated units (waggle runs), which repetitively transmit the same distance and direction vector from the nest. Intra-dance waggle run variation occurs and has been hypothesized as a colony-level adaptation to direct recruits over an area rather than a single location. Alternatively, variation may simply be due to constraints on bees' abilities to orient waggle runs. Here, we ask whether the angle at which the bee dances on vertical comb influences waggle run variation. In particular, we determine whether horizontal dances, where gravity is not aligned with the waggle run orientation, are more variable in their directional component. We analysed 198 dances from foragers visiting natural resources and found support for our prediction. More horizontal dances have greater angular variation than dances performed close to vertical. However, there is no effect of waggle run angle on variation in the duration of waggle runs, which communicates distance. Our results weaken the hypothesis that variation is adaptive and provide novel support for the constraint hypothesis.     

Control of the horizontal flight-course by air-current sense organs in Locusta migratoria

ABSTRACT. The role of the air-current sense organs of Locusta migratoria (the antennae and the hair fields on the frons and vertex of the head) in control of the horizontal flight-course in relation to the air was investigated in locusts flying tethered on a torque gauge. The antennae were apparently not of importance in the control of flight direction in the horizontal plane. If the hair fields were stimulated by an air current from either side, however, a torque on the vertical body axis was generated by the beating wings after a reaction time of at least 0.1 s. In free flight this would result in a yaw, bringing the animal back in line with the air stream. This torque reaction will stabilize the flight direction in the horizontal plane via a negative feedback mechanism, the hair fields above the lateral ocelli being the feedback receptors. In free flying locusts a torque on the vertical body axis can be generated by both the beating wings and the abdomen working as a rudder when bent to either side. The wings, however, are dominant in the reflex stabilization of the flight-course.     

Vibration Signal Behavior of Waggle-dancers in Swarms of the Honey Bee,Apis mellifera (Hymenoptera: Apidae)

We hypothesize two functions of the vibration signal (dorsal ventral abdominal vibration = DVAV) during swarming in honey bees: 1. it enhances recruitment to the specific sites advertised by the waggle dancers which also perform the vibration signal; and 2. it acts as a nonspecific modulatory signal to stimulate activity in other bees. The stimulation of activity invoked by the second hypothesis might include increasing nest-site scouting and dance following early in the house-hunting process or rousing quiescent bees to prepare them for lift-off late in the process, or both. In studies of neotropical African bee swarms in Costa Rica and European bees in California we tested these hypotheses by looking for associations between production of vibration signals by nest-site recruiters and site attractiveness (indicated by which site was ultimately chosen and by distance from the swarm since swarms may have a distance preference). Overall, bees dancing for the chosen sites performed vibration signals to the same extent as those dancing for the other sites. There were no distance differences between sites whose scouts did and did not vibrate other bees. These results are inconsistent with the hypothesis that the vibration signal enhances recruitment to especially high quality sites and they support the hypothesis that it plays a general excitatory role in the context of house hunting by swarming bees.     

Hydrocarbons Emitted by Waggle-Dancing Honey Bees Increase Forager Recruitment by Stimulating Dancing

Hydrocarbons emitted by waggle-dancing honey bees are known to reactivate experienced foragers to visit known food sources. This study investigates whether these hydrocarbons also increase waggle-dance recruitment by observing recruitment and dancing behavior when the dance compounds are introduced into the hive. If the hydrocarbons emitted by waggle-dancing bees affect the recruitment of foragers to a food source, then the number of recruits arriving at a food source should be greater after introduction of dance compounds versus a pure-solvent control. This prediction was supported by the results of experiments in which recruits were captured at a feeder following introduction of dance-compounds into a hive. This study also tested two nonexclusive behavioral mechanism(s) by which the compounds might stimulate recruitment; 1) increased recruitment could occur by means of increasing the recruitment effectiveness of each dance and/or 2) increased recruitment could occur by increasing the intensity of waggle-dancing. These hypotheses were tested by examining video records of the dancing and recruitment behavior of individually marked bees following dance-compound introduction. Comparisons of numbers of dance followers and numbers of recruits per dance and waggle run showed no significant differences between dance-compound and solvent-control introduction, thus providing no support for the first hypothesis. Comparison of the number of waggle-dance bouts and the number of waggle runs revealed significantly more dancing during morning dance-compound introduction than morning solvent-control introduction, supporting the second hypothesis. These results suggest that the waggle-dance hydrocarbons play an important role in honey bee foraging recruitment by stimulating foragers to perform waggle dances following periods of inactivity.     

Honeybee odometry: performance in varying natural terrain

Recent studies have shown that honeybees flying through short, narrow tunnels with visually textured walls perform waggle dances that indicate a much greater flight distance than that actually flown. These studies suggest that the bee's “odometer” is driven by the optic flow (image motion) that is experienced during flight. One might therefore expect that, when bees fly to a food source through a varying outdoor landscape, their waggle dances would depend upon the nature of the terrain experienced en route. We trained honeybees to visit feeders positioned along two routes, each 580 m long. One route was exclusively over land. The other was initially over land, then over water and, finally, again over land. Flight over water resulted in a significantly flatter slope of the waggle-duration versus distance regression, compared to flight over land. The mean visual contrast of the scenes was significantly greater over land than over water. The results reveal that, in outdoor flight, the honeybee's odometer does not run at a constant rate; rather, the rate depends upon the properties of the terrain. The bee's perception of distance flown is therefore not absolute, but scene-dependent. These findings raise important and interesting questions about how these animals navigate reliably.