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.     

What makes a honeybee scout?

A honeybee colony needs to divide its workforce so that each of the many tasks it performs has an appropriate number of workers assigned to it. This task allocation system needs to be flexible enough to allow the colony to quickly adapt to an ever-changing environment. In this study, we examined possible mechanisms by which a honeybee colony regulates the division of labor between scouts (foragers that search for new food sources without having been guided to them) and recruits (foragers that were guided via recruitment dances toward food sources). Specifically, we examined the roles that the availability of recruitment dances and worker genotype has in the colony-level regulation of the number of workers engaged in scouting. Our approach was threefold. We first developed a mathematical model to demonstrate that the decision to become a scout or a recruit could be regulated by whether a potential forager can find a recruitment dance within a certain time period. We then tested this model by investigating the effect of dance availability on the regulation of scouts in the field. Lastly, we investigated if the probability of being a scout has a genetic basis. Our field data supported the hypothesis that scouts are those foragers that have failed to locate a recruitment dance as predicted by our model, but we found no effect of genotype on the propensity of foragers to become scouts.     

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.     

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.

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.     

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 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     

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.     

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.     

Adaptation or constraint? Reference-dependent scatter in honey bee dances

The waggle dance of the honey bee is used to recruit nest mates to a resource. Dancer bees, however, may indicate many directions within a single dance bout; we show that this scatter in honey bee dances is strongly dependent on the sensory modality used to determine a reference angle in the dance. Dances with a visual reference are more precise than those with a gravity reference. This finding undermines the idea that scatter is introduced into dances, which the bees could perform more precisely, in order to spread recruits out over resource patches. It also calls into question reported interspecific differences that had been interpreted as adaptations of the dance to different habitats. Our results support a non-adaptive hypothesis: that dance scatter results from sensory and performance constraints, rather than modulation of the scatter by the dancing bee. However, an alternative adaptive hypothesis cannot be ruled out.     

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.     

The dance language of the honeybee mutant diminutive wings

Summary The dance communication of honeybees was studied using the short-winged mutant diminutive wings. The wing area of the mutant is reduced to 67% that of the wild type. This reduction in wing area leads to increases in both the wing beat frequency and the frequency of the sounds emitted during the dances. At the same time the amplitude of the sound signals is reduced. These changes have a strong effect on the recruitment success of the dances, which is reduced to less than 50%. Thus, the acoustical signals emitted by dancing bees play an essential role in the bees' dance communication.     

Tactics of dance choice in honey bees: do foragers compare dances?

Summary (1) When a honey bee follows recruitment dances to locate a new food source, does she sample multiple dances representing different food sources and selectively respond to the strongest dance? (2) Several initial findings suggested that foragers might indeed compare dances. First, dance information is arrayed in the hive in a way that facilitates comparison-making: dances for different flower patches are performed close together in time and space. Second, food-source quality is coded in the dances, in terms of dance length (number of circuits per dance). Third, dances to natural food sources vary in length by more than 2 orders of magnitude, indicating that the quality of natural food sources varies greatly. Fourth, foragers seeking a new food source follow several dances before exiting the hive (though only one dance is followed closely). (3) Nevertheless, a critical test for comparison-making revealed that foragers evidently do not compare dances. A colony was given two feeders that were equidistant from the hive but different in profitability. If foragers do not compare dances, then the proportion of recruits arriving at the richer feeder should match the proportion of dance circuits for the richer feeder. This is the pattern that we found in all 11 trials of the experiment. (4) We suggest that the reason foragers do not compare dances is that a colony's foraging success is greater if its foragers distribute themselves among the various food sources being advertised in the hive than if they crowd themselves on the one, best source. (5) Food-source selection by honey bee colonies is a democratic decision-making process. This study reveals that this selection process is organized to function effectively even though each member of the democracy possesses incomplete information about the available choices. Offprint requests to: T.D. Seeley     

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.     

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     

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.     

Exploration and exploitation of food sources by social insect colonies: a revision of the scout-recruit concept

Social insect colonies need to explore and exploit multiple food sources simultaneously and efficiently. At the individual level, this colony-level behaviour has been thought to be taken care of by two types of individual: scouts that independently search for food, and recruits that are directed by nest mates to a food source. However, recent analyses show that this strict division of labour between scouts and recruits is untenable. Therefore, a modified concept is presented here that comprises the possible behavioural states of an individual forager (novice forager, scout, recruit, employed forager, unemployed experienced forager, inspector and reactivated forager) and the transitions between them. The available empirical data are reviewed in the light of both the old and the new concept, and probabilities for the different transitions are derived for the case of the honey-bee. The modified concept distinguishes three types of foragers that may be involved in the exploration behaviour of the colony: novice bees that become scouts, unemployed experienced bees that scout, and lost recruits, i.e. bees that discover a food source other than the one to which they were directed to by their nest mates. An advantage of the modified concept is that it allows for a better comparison of studies investigating the different roles performed by social insect foragers during their individual foraging histories. Received: 29 December 1999 / Revised: 25 February 2000 / Accepted: 16 October 2000     

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.