Worker piping in honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): the behavior of piping nectar foragers

This study investigates the brief piping signals ("stop signals") of honey bee workers by exploring the context in which worker piping occurs and the identity and behavior of piping workers. Piping was stimulated reliably by promoting a colony's nectar foraging activity, demonstrating a causal connection between worker piping and nectar foraging. Comparison of the behavior of piping versus non-piping nectar foragers revealed many differences, e.g., piping nectar foragers spent more time in the hive, started to dance earlier, spent more time dancing, and spent less time on the dance floor. Most piping signals (approximately 99%) were produced by tremble dancers, yet not all (approximately 48%) tremble dancers piped, suggesting that the short piping signal and the tremble dance have related, but not identical, functions in the nectar foraging communication system. Our observations of the location and behavior of piping tremble dancers suggest that the brief piping signal may (1) retard recruitment to a low-quality food source, and (2) help to enhance the recruitment success of the tremble dance.     

Vibrational signals in the tremble dance of the honeybee,Apis mellifera

Summary The tremble dance is a behavior sometimes performed by honeybee foragers returning to the hive. The biological significance of this behavior was unclear until Seeley (1992) demonstrated that tremble dances occur mainly when a colony's nectar influx is so high that the foragers must undertake lenghty searches in order to find food storers to unload their nectar. He suggested that tremble dancing has the effect of stimulating additional bees to function as food-storers, thereby raising the colony's capacity for processing nectar. Here I describe vibrational signals emitted by the tremble dancers. Simulation experiments with artificial tremble dance sounds revealed that these sounds inhibited dancing and reduced recruitment to feeding sites. The results suggest that the tremble dance is a negative feedback system counterbalancing the positive feedback of recruitment by waggle dances. Thus, the tremble dance seems to affect not only the colony's nectar processing rate, but also its nectar intake rate.     

Worker allocation in insect societies: coordination of nectar foragers and nectar receivers in honey bee (Apis mellifera) colonies

Nectar collection in the honey-bee is partitioned. Foragers collect nectar and take it to the nest, where they transfer it to receiver bees who then store it in cells. Because nectar is a fluctuating and unpredictable resource, changes in worker allocation are required to balance the work capacities of foragers and receivers so that the resource is exploited efficiently. Honey bee colonies use a complex system of signals and other feedback mechanisms to coordinate the relative and total work capacities of the two groups of workers involved. We present a functional evaluation of each of the component mechanisms used by honey bees – waggle dance, tremble dance, stop signal, shaking signal and abandonment – and analyse how their interplay leads to group-level regulation. We contrast the actual regulatory system of the honey bee with theory. The tremble dance conforms to predicted best use of information, where the group in excess applies negative feedback to itself and positive feedback to the group in shortage, but this is not true of the waggle dance. Reasons for this and other discrepancies are discussed. We also suggest reasons why honey bees use a combination of recruitment plus abandonment and not switching between subtasks, which is another mechanism for balancing the work capacities of foragers and receivers. We propose that the waggle and tremble dances are the primary regulation mechanisms, and that the stop and shaking signals are secondary mechanisms, which fine-tune the system. Fine-tuning is needed because of the inherent unreliability of the cues, queueing delays, which foragers use to make recruitment decisions. Received: 15 December 1998 / Received in revised form: 6 March 1999 / Accepted: 12 March 1999     

Honey bee waggle dance communication: signal meaning and signal noise affect dance follower behaviour

Returning honey bee foragers perform waggle dances to inform nestmate foragers about the presence, location and odour of profitable food sources and new nest sites. The aim of this study is to investigate how the characteristics of waggle dances for natural food sources and environmental factors affect dance follower behaviour. Because food source profitability tends to decrease with increasing foraging distance, we hypothesised that the attractiveness of a dance, measured as the number of dance followers and their attendance, decreases with increasing distance to the advertised food location. Additionally, we determined whether time of year and dance signal noise, quantified as the variation in waggle run direction and duration, affect dance follower behaviour. Our results suggest that bees follow fewer waggle runs as the food source distance increases, but that they invest more time in following each dance. This is because waggle run duration increases with increasing foraging distance. Followers responded to increased angular noise in dances indicating more distant food sources by following more waggle runs per dance than when angular noise was low. The number of dance followers per dancing bee was also affected by the time of year and varied among colonies. Our results provide evidence that both noise in the message, that is variation in the direction component, and the message itself, that is the distance of the advertised food location, affect dance following. These results indicate that dance followers may pay attention to the costs and benefits associated with using dance information.     

Honeybee foragers adjust crop contents before leaving the hive

Upon leaving the hive, foragers carry a small amount of honey, which they subsequently consume to generate energy for flight. We investigated the relationship between waggle-phase duration and crop volume in foragers (both dancers and dance followers) leaving the hive. Our findings indicate that these variables were positively correlated in the two types of bee, suggesting that they were able to adjust the amount of food that they carry depending on the distance to a food source. We also found that dance followers left the hive with a larger amount of honey than dancers. We suggest two possible explanations: (1) dance followers have less information about the location of the food source than dancers, who have a better knowledge of the surrounding area; or (2) honeybees lack a precise calibration method for estimating energy needs from waggle-run duration. The effect of foraging experience was confirmed: bees decreased their honey load at departure with repeated trips to a sugar-syrup feeder. Honeybees showed a different pattern of change when the feeder provided soybean flour as a pollen substitute, possibly because honeybees use honey not only as an energy source but also as “glue” to form “balls” of pollen on their hind legs. Based on our observations that followers of sugar-syrup foragers carry a different amount of honey in their crop than followers of soybean-followers, we suggest that waggle dancers also convey information concerning food type.     

Floral scents affect the distribution of hive bees around dancers

Floral scents are important information cues used to organize foraging-related tasks in honeybees. The waggle dance, apart from encoding spatial information about food sources, might facilitate the transfer of olfactory information by increasing the dissipation of volatiles brought back by successful foragers. By assuming that food scents are more intensive on specific body parts of returning foragers, i.e., the posterior legs of pollen foragers and mouthparts of nectar foragers, we quantified the interactions between hive mates and foragers during dances advertising different types of food sources. For natural sources, a higher proportion of hive mates contacted the hind legs of pollen dancers (where the pollen loads were located) with their heads compared to non-pollen dancers. On the other hand, the proportion of head-to-head contacts was higher for non-pollen foragers during the waggle runs. When the food scent was manipulated, dancers collecting scented sugar solution had a higher proportion of head-to-head contacts and a lower proportion around their hind legs compared to dancers collecting unscented solution. The presence of food odors did not affect in-hive behaviors of dancers, but it increased the number of trophallaxes in-between waggle runs (i.e., during circle phases). These results suggest that the honeybee dance facilitates the olfactory information transfer between incoming foragers and hive mates, and we propose that excitatory displays in other social insect species serve the same purpose. While recent empirical and theoretical findings suggested that the colony level foraging benefits of the spatial information encoded in the waggle dance vary seasonally and with habitats, the role of the dance as a compound signal not only indicating the presence of a profitable resource but also amplifying the information transfer regarding floral odors may be important under any ecological circumstances.     

The honey bee shaking signal: function and design of a modulatory communication signal

This study explores the meaning and functional design of a modulatory communication signal, the honey bee shaking signal, by addressing five questions: (I) who shakes, (II) when do they shake, (III) where do they shake, (IV) how do receivers respond to shaking, and (V) what conditions trigger shaking. Several results confirm the work of Schneider (1987) and Schneider et al. (1986a): (I) most shakers were foragers (at least 83%); (II) shaking exhibited a consistent temporal pattern with bees producing the most signals in the morning (0810–1150 hours) just prior to a peak in waggle dancing activity; and (IV) bees moved faster (by 75%) after receiving a shaking signal. However, this study differs from previous work by providing a long-term, temporal, spatial, and vector analysis of individual shaker behavior. (III) Bees producing shaking signals walked and delivered signals in all areas of the hive, but produced the most shaking signals directly above the waggle dance floor. (IV) Bees responded to the signal by changing their direction of movement. Prior to receiving a signal, bees selected from the waggle dance floor moved, on average, towards the hive exit. After receiving a signal, some bees continued moving towards the exit but others moved directly away from the exit. During equivalent observation periods, non-shaken bees exhibited a strong tendency to move towards the hive exit. (V) Renewed foraging activity after food dearth triggered shaking signals, and, the level of shaking is positively correlated with the duration of food dearth. However, shaking signal levels also increased in the morning before foraging had begun and in the late afternoon after foraging had ceased. This spontaneous afternoon peak has not previously been reported. The shaking signal consequently appears to convey the general message “reallocate labor to different activities” with receiver context specifying a more precise meaning. In the context of foraging, the shaking signal appears to activate (and perhaps deactivate) colony foraging preparations. The generally weak response elicited by modulatory signals such as the shaking signal may result from a high receiver response threshold which allows the receiver to integrate multiple sources of information and which thereby increases the probability that receiver actions will be appropriate to colony needs. Received: 21 March 1997 / Accepted after revision: 30 August 1997     

The use of waggle dance information by honey bees throughout their foraging careers

We studied the extent to which worker honey bees acquire information from waggle dances throughout their careers as foragers. Small groups of foragers were monitored from time of orientation flights to time of death and all in-hive behaviors relating to foraging were recorded. In the context of a novice forager finding her first food source, 60% of the bees relied, at least in part, on acquiring information from waggle dances (being recruited) rather than searching independently (scouting). In the context of an experienced forager whose foraging has been interrupted, 37% of the time the bees resumed foraging by following waggle dances (being reactivated) rather than examining the food source on their own (inspecting). And in the context of an experienced forager engaged in foraging, 17% of the time the bees initiated a foraging trip by following a waggle dance. Such dance following was observed much more often after an unsuccessful than after a successful foraging trip. Successful foragers often followed dances just briefly, perhaps to confirm that the kind of flowers they had been visiting were still yielding forage. Overall, waggle dance following for food discovery accounted for 12–25% of all interactions with dancers (9% by novice foragers and 3–16% by experienced foragers) whereas dance following for reactivation and confirmation accounted for the other 75–88% (26% for reactivation and 49–62% for confirmation). We conclude that foragers make extensive use of the waggle dance not only to start work at new, unfamiliar food sources but also to resume work at old, familiar food sources.     

The role of the vibration signal in the house-hunting process of honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) swarms

The function of the vibration signal of the honey bee (Apis mellifera) during house hunting was investigated by removing vibrating bees from swarms and examining the effects on waggle dancing for nest sites, liftoff preparations and swarm movement. We compared house hunting among three swarm types: (1) test swarms (from which vibrating bees were removed), (2) manipulated control (MC) swarms (from which randomly selected workers and some waggle dancers were removed), and (3) unmanipulated control (UC) swarms (from which no bees were removed). The removal of vibrating bees had pronounced effects on liftoff preparations and swarm movement. Compared to the MC and UC swarms, the test swarms had significantly greater liftoff-preparation periods, were more likely to abort liftoff attempts, and in some cases were unable to move to the chosen site after the swarm became airborne. However, the three swarm types did not differ in overall levels of waggle dance activity, the time required to achieve consensus for a nest site, the rate at which new waggle dancers were recruited for the chosen site, or the ability to maintain levels of worker piping necessary to prepare for flight. The removal of vibrating bees may therefore have altered liftoff behavior because of a direct effect on vibration signal activity. A primary function of the signal during house hunting may be to generate a level of activity in workers that enhances and coordinates responses to other signals that stimulate departure and movement to a new location.Communicated by R. Page     

The occurrence and context of tremble dancing in free-foraging honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Nectar foraging in honey bees is regulated by several communication signals that are performed mainly by foragers. One of these signals is the tremble dance, which is consistently performed by foragers from a rich food source which, upon return to the hive, experience a long delay before unloading their nectar to a nectar receiver. Although tremble dancing has been studied extensively using artificial nectar sources, its occurrence and context in a more natural setting remain unknown. Therefore, this study tests the sufficiency of the current explanations for tremble dancing by free-foraging honey bees. The main finding is that only about half of the observations of tremble dancing, referred to as delay-type tremble dancing, are a result of difficulty in finding a nectar receiver. In the remaining observations, tremble dancing was initiated immediately upon entering the hive, referred to as non-delay-type tremble dancing. Non-delay tremble dancing was associated with first foraging successes, both in a forager's career and in a single day. More than 75% of tremble dancing was associated with good foraging conditions, as indicated by the dancer continuing to forage after dancing. However, at least some of the other cases were associated with deteriorated foraging conditions, such as the end of the day, after which foraging was discontinued. No common context could be identified that explains all cases of tremble dancing or the subset of non-delay-type tremble dancing. This study shows that the current explanations for the cause of the tremble dance are insufficient to explain all tremble dancing in honey bees that forage at natural food sources.     

Honey bee foragers as sensory units of their colonies

Forager honey bees function not only as gatherers of food for their colonies, but also as sensory units shaped by natural selection to gather information regarding the location and profitability of forage sites. They transmit this information to colony members by means of waggle dances. To investigate the way bees transduce the stimulus of nectar-source profitability into the response of number of waggle runs, I performed experiments in which bees were stimulated with a sucrose solution feeder of known profitability and their dance responses were videorecorded. The results suggest that several attributes of this transduction process are adaptations to enhance a bee's effectiveness in reporting on a forage site. (1) Bees register the profitability of a nectar source not by sensing the energy gain per foraging trip or the rate of energy gain per trip, but evidently by sensing the energetic efficiency of their foraging. Perhaps this criterion of nectar-source profitability has been favored by natural selection because the foraging gains of honey bees are typically limited by energy expenditure rather than time availability. (2) There is a linear relationship between the stimulus of energetic efficiency of foraging and the response of number of waggle runs per dance. Such a simple stimulus-response function appears adequate because the range of suprathreshold stimuli (max/min ratio of about 10) is far smaller than the range of responses (max/min ratio of about 100). Although all bees show a linear stimulus-response function, there are large differences among individuals in both the response threshold and the slope of the stimulus-response function. This variation gives the colony a broader dynamic range in responding to food sources than if all bees had identical thresholds of dance response. (3) There is little or no adaptation in the dance response to a strong stimulus (tonic response). Thus each dancing bee reports on the current level of profitability of her forage site rather than the changes in its profitability. This seems appropriate since presumably it is the current profitability of a forage site, not the change in its profitability, which determines a site's attractiveness to other bees. (4) The level of forage-site quality that is the threshold for dancing is tuned by the bees in relation to forage availability. Bees operate with a lower dance threshold when forage is sparse than when it is abundant. Thus a colony utilizes input about a wide range of forage sites when food is scarce, but filters out input about low-reward sites when food is plentiful. (5) A dancing bee does not present her information in one spot within the hive but instead distributes it over much of the dance floor. Consequently, the dances for different forage sites are mixed together on the dance floor. This helps each bee following the dances to take a random sample of the dance information, which is appropriate for the foraging strategy of a honey bee colony since it is evidently designed to allocate foragers among forage sites in proportion to their profitability.     

The causes of the tremble dance of the honeybee,Apis mellifera

Tremble dances are sometimes performed by returning forager bees instead of waggle dances. Recent studies by Seeley (1992) and Kirchner (1993) have revealed that this behaviour is part of the recruitment communication system of bees. The ultimate cause of tremble dances is, according to Seeley (1992), an imbalance between the nectar intake rate and the nectar processing capacity of the colony. This imbalance is correlated with a long initial search time of returning foragers to find bees to unload them. However, it remained unclear whether a long search time is the direct proximate cause of tremble dancing. Here we report that a variety of experimental conditions can elicit tremble dances. All of them have in common that the total search time that foragers spend searching for unloaders, until they are fully unloaded, is prolonged. This finding supports and extends the hypothesis that a long search time is the proximate cause of tremble dancing. The results also confirm the previous reports of Lindauer (1948) and others about factors eliciting tremble dancing.     

Does a polyandrous honeybee queen improve through patriline diversity the activity of her colony’s scouting foragers?

Recent studies indicate that the foraging success of a honeybee colony is enhanced when it has numerous genetically diverse patrilines because of queen polyandry. We determined whether foraging is improved in part because patriline diversity generates more responsive populations of scouting foragers. Scouts search for new food sources and advertise them with waggle dances to inform other foragers about unexploited discoveries. We moved multiple-patriline and single-patriline colonies to unfamiliar locations so that colonies relied heavily on successful scouts to initiate recruitment and then compared the development of foraging effort between the two types of colonies. More waggle dance signals were produced during the incipient stages of foraging in multiple-patriline colonies compared to single-patriline colonies because scouts reported food discoveries with longer dances. Scouts also returned to multiple-patriline colonies at rates that were two thirds higher than those of single-patriline colonies, although return rates for general forager populations were not significantly different between colony types. The distance of reported food sources from hives increased with time for all colonies, but by the end of their first day in an unfamiliar environment, maximal foraging reach was greater if colonies had multiple patrilines. Most scouts in multiple-patriline colonies came from a minority of scout-rich patrilines that were generally not those from which general forager populations were derived; the presence of such scout-rich patrilines was correlated with the extent of recruitment signaling in colonies. We show how a honeybee colony’s scouting effort is (and is not) enhanced when extremely polyandrous queens produce genetically diverse colonies.     

Do honey bees average directions in the waggle dance to determine a flight direction?

The waggle dance of the honey bee is a recruitment behavior used to communicate the location of a resource to a nest mate. There is, however, significant imprecision communicating the direction across waggle runs in a single dance. In this study, we ask whether honey bee recruits determine the direction of their flight based on an average of many waggle runs, or on a single waggle run. We show that the distribution of recruit flight directions is narrower than the distribution of directions indicated in the dance. We also show that there is a better fit between observed flight directions and the prediction of a multiple-waggle-run-averaging model than a last-waggle-run or other single-waggle-run models. These findings substantially weaken hypotheses about the adaptive nature of imprecision in honey bee recruitment.     

The honey bee’s tremble dance stimulates additional bees to function as nectar receivers

If a forager bee returns to her hive laden with high-quality nectar but then experiences difficulty finding a receiver bee to unload her, she will begin to produce a conspicuous communication signal called the tremble dance. The context in which this signal is produced suggests that it serves to stimulate more bees to function as nectar receivers, but so far there is no direct evidence of this effect. We now report an experiment which shows that more bees do begin to function as nectar receivers when foragers produce tremble dances. When we stimulated the production of tremble dances in a colony and counted the number of bees engaged in nectar reception before and after the period of intense tremble dancing, we found a dramatic increase. In two trials, the number of nectar receivers rose from 17% of the colony’s population before tremble dancing to 30–50% of the population after the dancing. We also investigated which bees become the additional nectar receivers, by looking at the age composition of the receiver bees before and after the period of intense tremble dancing. We found that none of the bees recruited to the task of nectar reception were old bees, most were middle-aged bees, and some were even young bees. It remains unclear whether these auxiliary nectar receivers were previously inactive (as a reserve supply of labor) or were previously active on other tasks. Overall, this study demonstrates that a honey bee colony is able to rapidly and strongly alter its allocation of labor to adapt to environmental changes, and it further documents one of the communication mechanisms underlying this ability. Received: 31 May 1996/Accepted after revision: 9 August 1996     

Promiscuous honeybee queens generate colonies with a critical minority of waggle-dancing foragers

Honeybees present a paradox that is unusual among the social Hymenoptera: extremely promiscuous queens generate colonies of nonreproducing workers who cooperate to rear reproductives with whom they share limited kinship. Extreme polyandry, which lowers relatedness but creates within-colony genetic diversity, produces substantial fitness benefits for honeybee queens and their colonies because of increased disease resistance and workforce productivity. However, the way that these increases are generated by individuals in genetically diverse colonies remains a mystery. We assayed the foraging and dancing performances of workers in multiple-patriline and single-patriline colonies to discover how within-colony genetic diversity, conferred to colonies by polyandrous queens, gives rise to a more productive foraging effort. We also determined whether the initiation by foragers of waggle-dance signaling in response to an increasing sucrose stimulus (their dance response thresholds) was linked to patriline membership. Per capita, foragers in multiple-patriline colonies visited a food source more often and advertised it with more waggle-dance signals than foragers from single-patriline colonies, although there was variability among multiple-patriline colonies in the strength of this difference. High-participation patrilines emerged within multiple-patriline colonies, but their more numerous foragers and dancers were neither more active per capita nor lower-threshold dancers than their counterparts from low-participation patrilines. Our results demonstrate that extreme polyandry does not enhance recruitment effort through the introduction of low-dance-threshold, high-activity workers into a colony’s population. Rather, genetic diversity is critical for injecting into a colony’s workforce social facilitators who are more likely to become engaged in foraging-related activities, so boosting the production of dance signals and a colony’s responsiveness to profitable food sources.     

Imprecision in waggle dances of the honeybee (Apis mellifera) for nearby food sources: error or adaptation?

A curious feature of the honeybee's waggle dance is the imprecision in the direction indication for nearby food sources. One hypothesis for the function of this imprecision is that it serves to spread recruits over a certain area and thus is an adaptation to the typical spatial configuration of the bees' food sources, i.e., flowers in sizable patches. We report an experiment that tests this tuned-error hypothesis. We measured the precision of direction indication in waggle dances advertising a nest site (typically a tree cavity, hence a target that is almost a point) and compared it with that of dances advertising a food source (typically a flower patch, hence a target that covers an area). The precision of dances for a nearby nest site was significantly higher than that of dances for an equidistant feeder. This was demonstrated four times with four colonies. Our evidence therefore supports the hypothesis that the level of precision in the direction indication for nearby food sources is tuned to its optimum without being at its maximum. Received: 9 December 1998 / Received in revised form: 24 February 1999 / Accepted 12 March 1999     

Acoustical signals in the dance language of the giant honeybee,Apis dorsata

Summary Acoustical signals emitted by dancing bees have recently been shown to transmit information about the location of food sources in the western honeybee, Apis mellifera. Towne (1985) reported that in the Asian honeybee species Apis dorsata, which builds a single comb in the open under overhanging rocks or tree branches, sound signals were not emitted by the dancers. This led to the conclusion that acoustical communication is restricted to bees that nest in the dark, like A. mellifera. Here we show that in fact A. dorsata produces dance sounds similar to those emitted by A. mellifera, and that these acoustical signals contain information about distance, direction and profitability of food sources. The acoustical transfer of information has thus evolved independently of nesting in dark cavities. The significance of nocturnal activity in Apis dorsata for the evolution of sound communication is discussed. Correspondence to: W.H. Kirchner     

The tremble dance of the honey bee: message and meanings

Summary The nectar foragers of a honey bee colony, upon return to the hive, sometimes perform a mysterious behavior called the tremble dance. In performing this dance, a forager shakes her body back and forth, at the same time rotating her body axis by about 50° every second or so, all the while walking slowly across the comb. During the course of a dance, which on average lasts 30 min, the bee travels about the broodnest portion of the hive. It is shown experimentally that a forager will reliably perform this dance if she visits a highly profitable nectar source but upon return to the hive experiences great difficulty finding a food-storer bee to take her nectar. This suggests that the message of the tremble dance is I have visited a rich nectar source worthy of greater exploitation, but already we have more nectar coming into the hive than we can handle. It is also shown experimentally that the performance of tremble dances is followed quickly by a rise in a colony's nectar processing capacity and (see Nieh, in press and Kirchner, submitted) by a drop in a colony's recruitment of additional bees to nectar sources. These findings suggest that the tremble dance has multiple meanings. For bees working inside the hive, its meaning is apparently I should switch to the task of processing nectar, while for bees working outside the hive (gathering nectar), its meaning is apparently I should refrain from recruiting additional foragers to my nectar source. Hence it appears that the tremble dance functions as a mechanism for keeping a colony's nectar processing rate matched with its nectar intake rate at times of greatly increased nectar influx. Evidently the tremble dance restores this match in part by stimulating a rise in the processing rate, and in part by inhibiting any further rise in the intake rate. Correspondence to: T. Seeley