Consensus building during nest-site selection in honey bee swarms: the expiration of dissent

This study addresses a question that lies at the heart of understanding how the scouts in a honey bee swarm achieve unanimity in their dances, and so reach agreement in their choice of a future nest site: what causes the scouts that perform dances for the non-chosen sites to stop dancing for these sites? One possibility is that a scout stops dancing for a non-chosen site only after she follows a lively dance for another site, such as the site that is ultimately chosen. This hypothesis is contradicted by the finding that 23 out of 27 scouts (in 6 swarms) that danced initially for a non-chosen site stopped their dancing before they followed a dance for another site. Evidently, a scout that supports initially one of the non-chosen sites is likely to withdraw her support for this site even before she learns about another site. What causes her to do so? Close examination of the behavior of scouts revealed that they reduce the strength of their dancing (waggle runs/return to the swarm) for a given site over consecutive returns to the swarm. On average, the pattern of this reduction in dancing is strikingly linear, which suggests that it arises from an internal, neurophysiological process that automatically drives down a scout's motivation to dance for a site. Other results suggest that scouts from inferior sites start their dancing less strongly, and so cease their dancing more rapidly, than do scouts from superior sites. If so, then during the consensus-building process of the scouts, it is the support (the dancing) for inferior sites that is most likely to die out while it is the support for a superior site that is most likely to prevail.     

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     

Quorum sensing during nest-site selection by honeybee swarms

This study addresses a question about the nest-site selection process of honeybee swarms: how do the scout bees know when to initiate the preparation for their swarm’s move to their new home? We tested the quorum-sensing hypothesis: that the scouts do this by noting when one of the potential nest sites under consideration is being visited by a sufficiently large number of scouts. A falsifiable prediction of this hypothesis is that delaying the formation of a quorum of scout bees at a swarm’s chosen nest cavity, while leaving the rest of the decision-making process undisturbed, should delay the start of worker piping (the prepare-for-takeoff signal) and thus the takeoff of the swarm. In paired trials, we presented each of four swarms once with five nest boxes close to each other at a site and once with a single nest box. The multiple nest boxes caused the scouts visiting the site to be dispersed among five identical nest cavities rather than concentrated at one. We observed long delays in the start of piping and the start of takeoff in the five-nest-box trials relative to the one-nest-box trials. These results provide strong support for the quorum-sensing hypothesis.     

Nest-site selection in honey bees: how well do swarms implement the "best-of-N" decision rule?

This study views a honey bee swarm as a supraorganismal entity which has been shaped by natural selection to be skilled at choosing a future home site. Prior studies of this decision-making process indicate that swarms attempt to use the best-of-N decision rule: sample some number (N) of alternatives and then select the best one. We tested how well swarms implement this decision rule by presenting them with an array of five nest boxes, only one of which was a high-quality (desirable) nest site; the other four were medium-quality (acceptable) sites. We found that swarms are reasonably good at carrying out the best-of-N decision rule: in four out of five trials, swarms selected the best site. In addition, we gained insights into how a swarm implements this decision rule. We found that when a scout bee returns to the swarm cluster and advertises a potential nest site with a waggle dance, she tunes the strength of her dance in relation to the quality of her site: the better the site, the stronger the dance. A dancing bee tunes her dance strength by adjusting the number of waggle-runs/dance, and she adjusts the number of waggle-runs/dance by changing both the duration and the rate of her waggle-run production. Moreover, we found that a dancing bee changes the rate of her waggle-run production by changing the mean duration of the return-phase portion of her dance circuits. Differences in return-phase duration underlie the impression that dances differ in liveliness. Although a honey bee swarm has bounded rationality (e.g., it lacks complete knowledge of the possible nesting sites), through its capacity for parallel processing it can choose a nest site without greatly reducing either the breadth or depth of its consideration of the alternative sites. Such thoroughness of information gathering and processing no doubt helps a swarm implement the best-of-N decision rule.     

Nest site selection in the open-nesting honeybee Apis florea

We studied nest site selection by swarms of the red dwarf honeybee, Apis florea. By video recording and decoding all dances of four swarms, we were able to determine the direction and distances indicated by 1,239 dances performed by the bees. The bees also performed a total of 715 nondirectional dances; dances that were so brief that no directional information could be extracted. Even though dances converged over time to a smaller number of areas, in none of the swarms did dances converge to one site. As a result, even prior to lift off, bees performed dances indicating nest sites in several different directions. Two of four swarms traveled directly in what seemed to be the general direction indicated by the majority of dances in the half hour prior to swarm lift off. The other two traveled along circuitous routes in the general direction indicated by the dances. We suggest that nest site selection in A. florea has similar elements to nest site selection in the better-studied Apis mellifera. However, the observation that many more locations are indicated by dances prior to lift off also shows that there are fundamental differences between the two species.     

Choosing a home: how the scouts in a honey bee swarm perceive the completion of their group decision making

This study considers the mystery of how the scout bees in a honey bee swarm know when they have completed their group decision making regarding the swarm's new nest site. More specifically, we investigated how the scouts sense when it is appropriate for them to begin producing the worker piping signals that stimulate their swarm-mates to prepare for the flight to their new home. We tested two hypotheses: "consensus sensing," the scouts noting when all the bees performing waggle dances are advertising just one site; and "quorum sensing," the scouts noting when one site is being visited by a sufficiently large number of scouts. Our test involved monitoring four swarms as they discovered, recruited to, and chose between two nest boxes and their scouts started producing piping signals. We found that a consensus among the dancers was neither necessary nor sufficient for the start of worker piping, which indicates that the consensus sensing hypothesis is false. We also found that a buildup of 10–15 or more bees at one of the nest boxes was consistently associated with the start of worker piping, which indicates that the quorum sensing hypothesis may be true. In considering why the scout bees rely on reaching a quorum rather than a consensus as their cue of when to start preparing for liftoff, we suggest that quorum sensing may provide a better balance between accuracy and speed in decision making. In short, the bees appear to begin preparations for liftoff as soon as enough of the scout bees, but not all of them, have approved of one of the potential nest sites.

Consistent personality differences in house-hunting behavior but not decision speed in swarms of honey bees (<Emphasis Type="BoldItalic">Apis mellifera</Emphasis>)

Speed-accuracy tradeoffs are a common feature of decision-making processes, both in individual animals and in groups of animals working together to reach a single collective decision. Individual organisms display consistent differences in their “impulsivity,” and vary in their tendency to make rapid, impulsive choices as opposed to slower, more accurate decisions. However, we do not yet know whether groups of animals consistently differ in their tendency to prioritize decision speed over accuracy. We challenged 17 swarms of honey bees (Apis mellifera) to simultaneously choose a new nest site in each of three locations, and measured their decision speeds in each trial. We found that swarms displayed consistent personality differences in the number of waggle dances and shaking signals they performed and in how actively they scouted for new nest sites. However, swarms did not consistently differ in how long they took to choose a nest site. We suggest that house-hunting A. mellifera swarms may place an especially high emphasis on decision accuracy when choosing a nest site, and that chance events—such as the time when each swarm discovers a sufficiently high-quality nest site—may consequently play a greater role in determining a swarm’s decision speed than intrinsic characteristics such as a swarm’s “impulsivity.”     

Moving home: nest-site selection in the Red Dwarf honeybee (<Emphasis Type="Italic">Apis florea</Emphasis>)

The Red Dwarf honeybee (Apis florea) is one of two basal species in the genus Apis. A. florea differs from the well-studied Western Hive bee (Apis mellifera) in that it nests in the open rather than in cavities. This fundamental difference in nesting biology is likely to have implications for nest-site selection, the process by which a reproductive swarm selects a new site to live in. In A. mellifera, workers show a series of characteristic behaviors that allow the swarm to select the best nest site possible. Here, we describe the behavior of individual A. florea workers during the process of nest-site selection and show that it differs from that seen in A. mellifera. We analyzed a total of 1,459 waggle dances performed by 197 scouts in five separate swarms. Our results suggest that two fundamental aspects of the behavior of A. mellifera scouts—the process of dance decay and the process of repeated nest site evaluation—do not occur in A. florea. We also found that the piping signal used by A. mellifera scouts to signal that a quorum has been reached at the chosen site, is performed by both dancing and non-dancing bees in A. florea. Thus, the piping signal appears to serve a different purpose in A. florea. Our results illustrate how differences in nesting biology affect the behavior of individual bees during the nest-site selection process.     

The modulation of worker behavior by the vibration signal during house hunting in swarms of the honeybee, Apis mellifera

During house hunting, honeybee, Apis melli- fera, workers perform the vibration signal, which may function in a modulatory manner to influence several aspects of nestsite selection and colony movement. We examined the role of the vibration signal in the house-hunting process of seven honeybee swarms. The signal was performed by a small proportion of the older bees, and 20% of the vibrating bees also performed waggle dances for nestsites. Compared to non-vibrating controls, vibrating bees exhibited increased rates of locomotion, were more likely to move into the interiors of the swarms, and were more likely to fly from the clusters and perform waggle dances. Recipients responded to the signal with increased locomotion and were more likely than non- vibrated controls to fly from the swarms. Because vibration signals were intermixed with waggle dances by some vibrators, and because they stimulated flight in recipients, the signals may have enhanced nestsite scouting and recruitment early in the house-hunting process. All swarms exhibited increased vibration activity within 0.5–1 h of departure. During these final periods, numerous vibrating bees wove repeatedly in and out of the clusters while signaling and motion on the swarms increased until it culminated in mass flight. The peaks of vibration activity observed at the end of the house-hunting process may therefore have activated the entire swarm for liftoff once a new nestsite had been selected. Thus, the vibration signal may help to integrate the behavior of numerous groups of workers during nestsite selection and colony relocation. Received: 17 January 2000 / Received in revised form: 5 April 2000 / Accepted: 3 May 2000     

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.     

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.     

Coordinating a group departure: who produces the piping signals on honeybee swarms?

A swarm of honeybees provides a striking example of an animal group performing a synchronized departure for a new location; in this case, thousands of bees taking off at once to fly to a new home. However, the means by which this is achieved remain unclear. Shortly before takeoff, one hears a crescendo of a high-pitched mechanical signal—worker piping—so we explored the role of this signal in coordinating a swarm’s mass takeoff. Specifically, we examined whether exclusively nest site scouts produce the worker piping signal or whether it is produced in a relay or chain reaction fashion. We found no evidence that bees other than the scouts that have visited the swarm’s chosen nest site produce piping signals. This absence of relay communication in piping suggests that it is a signal that only primes swarms for takeoff and that the release of takeoff is triggered by some other signal or cue; perhaps the takeoff of bees on the swarm periphery as they reach flight temperature in response to piping.     

Modeling and analysis of nest-site selection by honeybee swarms: the speed and accuracy trade-off

Nest-site selection in honeybees is a process of social decision making in which the scout bees in a swarm locate several potential nest sites, evaluate them, and select the best one by means of competitive signaling. We develop a model of this process and validate that the model possesses the key features of the bees' decision-making process, as revealed by prior empirical studies. Next, we use the model to study the “design” of the nest-site selection process, with a focus on how certain behavioral parameters have been tuned by natural selection to achieve a balance between speed and accuracy. First, we study the effects of the quorum threshold and the dance decay rate. We show that evolution seems to have settled on values for these two parameters that seek a balance between speed and accuracy of decision making by minimizing the time needed to achieve a consensus and maximizing the probability that the best site is chosen. Second, we study the adaptive tuning of the tendency of bees to explore for vs be recruited to a site. We show that this tendency appears to be tuned to regulate the positive feedback process of recruitment to ensure both a reasonably rapid choice and a low probability of a poor choice. Finally we show that the probability of choosing the best site is proportional to its quality, but that this proportionality depends on its quality relative to other discovered sites.

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.     

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     

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.     

Dance precision of <Emphasis Type="Italic">Apis florea</Emphasis>—clues to the evolution of the honeybee dance language?

All honeybee species make use of the waggle dance to communicate the direction and distance to both food sources and potential new nest sites. When foraging, all species face an identical problem: conveying information about profitable floral patches. However, profound differences in nesting biology (some nest in cavities while others nest in the open, often on a branch or a cliff face) may mean that species have different requirements when dancing to advertise new nest sites. In cavity nesting species, nest sites are a precise location in the landscape: usually a small opening leading to a cavity in a hollow tree. Dances for cavities therefore need to be as precise as possible. In contrast, when the potential nest site comprises a tree or perhaps seven a patch of trees, precision is less necessary. Similarly, when a food patch is advertised, dances need not be very precise, as floral patches are often large, unless they are so far away that recruits need more precise information to be able to locate them. In this paper, we study the dance precision of the open-nesting red dwarf bee Apis florea. By comparing the precision of dances for food sources and nest sites, we show that A. florea workers dance with the same imprecision irrespective of context. This is in sharp contrast with the cavity-nesting Apis mellifera that increases the precision of its dance when advertising a potential new home. We suggest that our results are in accordance with the hypothesis that the honeybees’ dance communication initially evolved to convey information about new nest sites and was only later adapted for the context of foraging.     

Mate choice tactics and swarm size: a model and a test in a dance fly

In the dance flyEmpis borealis (L.) (Diptera: Empididae) females gather to swarm and males visit swarms for mating. A model was constructed, based on previously published data, simulating how males may choose among females of different sizes in swarms of different sizes. The focal question was, what influences the number of individuals in the swarm in this and possibly other swarming insects? The relationships between original swarm size and both the number of males arriving per minute and the proportion of males mating are both logarithmic. The model predicted that if these relationships were linear, or if males were able to judge absolute female size, the mean swarm size should increase and be at least four times as large as those found in the field. The only type of male mate choice strategy that gave rise to very large swarms (>25) was size-related choice (if males are able to assess the size of a female in relation to the entire population and not merely to the swarm). Furthermore, no swarming behaviour would occur if males mate independently of swarm size. Thus, the numbers of females attending a given swarm site are influenced by male arrival pattern, male preference for larger swarms, the inability of males to judge the absolute body size of females, and female polyandry. Males searching for mates seem to prefer larger swarms than females searching for a swarm to join, but the mean swarm size is primarily set by the swarm size preference of females. Optimal swarm size predicted from the model was 4.68±0.53 females. In order to test model predictions, 69 natural swarm sites were studied during one season. The mean swarm size was 4.85±4.54 females (median 4.03), and about 90% of swarms consisted of 11 females or fewer. Predicted and observed swarm size did not differ significantly.     

Why insects swarm: testing the models for lek mating systems on swarming Empis borealis females

Summary Female dance-flies, Empis borealis L., gather to swarm, and males carrying nuptial gifts visit swarms for mating. Field observations and experiments were performed on this behaviorally sex-role reversed species to test models of lekking behavior. The key predictions were: (1) female preference model: male visiting rate and mating rate should increase with the number of females in swarm (swarm size), (2) hotspot model: male visiting rate should be independent of swarm size, and (3) hotshot model: swarm size should be positively correlated with the body size of the largest female in swarm. We found that male visiting rate and mating rate increased with swarm size, and that mating rate per female increased with swarm size. Males also mated more often in larger swarms than in smaller ones. Both males and females visited swarm sites even in the absence of other individuals. When females were successively removed from swarm sites more males than females on average arrived at these sites: 2.25 males per female. When no individuals were present at the swarm site, arriving males moved on to another site, whereas arriving females generally stayed. Larger experimental swarm-markers attracted both more males and more females and even more males when swarming females were present. There was no correlation between mean or median female size in swarms and the number of females in swarms. Thus, the female preference model and the hotspot model were corroborated, while other models were judged unlikely to explain swarming behavior in E. borealis. Correspondence to: B.G. Svensson     

Modelling collective foraging by means of individual behaviour rules in honey-bees

An individual-oriented model is constructed which simulates the collective foraging behaviour of a colony of honey-bees, Apis mellifera. Each bee follows the same set of behavioural rules. Each rule consists of a set of conditions followed by the behavioural act to be performed if the conditions are fulfilled. The set of conditions comprises the state of external information available to the bee (e.g. the dancing of other bees) and internal information variables (like memorised location of a food source and homing motivation). The rules are partly observational (i.e. they capture the observable regularities between the present external information and the individual bee's behaviour), and partly involve hypothesised internal-state variables (e.g. abandoning tendency and homing motivation), because no observable (physiological) aspect has as yet been detected in the bee which correlates with changes in the internal motivation. Our aim is to obtain a set of rules that is necessary and sufficient for the generation of the collective foraging behaviour observed in real bees. We simulated an experiment performed by Seeley et al. in which a colony of honey-bees chooses between two nectar sources of different profitabilities which are switched at intervals. A good fit between observed and simulated collective forager patterns was obtained when the model included rules in which the bees (1) relied on the information acquired from previous flights to a source (e.g. profitability and time of day when the source was found), (2) used positional information obtained by attending recruitment dances and (3) did not abandon a (temporarily) deteriorated source too fast or too slowly. The significance of the following issues is discussed: the role of internal and external information, source profitability, the spatial precision of the dance communication, the ability to search for a source after the source position has been transmitted, the tendency to abandon a deteriorated source, and the concepts of scout, recruit, (un)employed forager, and foraging history. Received: 26 January 1998 / Accepted after revision: 16 May 1998