The buzz-run: how honeybees signal ‘Time to go!’

ANIMAL BEHAVIOUR, 2008, 75, 189e197 doi:10.1016/j.anbehav.2007.04.026

Available online at www.sciencedirect.com

The buzz-run: how honeybees signal ‘Time to go!’ CL ARE C . R ITT SC HOF * & THOMAS D. SEELEY †

*Department of Zoology, University of Florida yDepartment of Neurobiology and Behavior, Cornell University (Received 7 February 2007; acceptance 27 April 2007; MS. number: A10688)

The explosive take-off of a honeybee swarm when it moves to its new home is a striking example of an animal group performing a synchronized departure for a new location. Prior work has shown that the nest-site scouts in a swarm prime the other bees for flight by producing piping signals that stimulate all the bees to warm up their wing muscles in preparation for flight, but how the bees are ultimately triggered to take flight remains a mystery. We explored the possibility that the buzz-run signal is the critical releaser of flight. Using slow-motion analyses of videorecordings, we made a detailed description of this signalling behaviour: a buzz-runner runs about the swarm cluster in great excitement, tracing out a crooked path, buzzing her wings in bursts, bulldozing between idle bees and periodically performing a conspicuous wiggling movement. It seems likely that the buzz-run signal is a ritualized form of a bee’s take-off behaviour, with the wing buzzing greatly exaggerated and other behavioural elements (running, butting and wiggling) added to increase the signal’s detectability. The immediate effect of the signal is to disperse and activate otherwise lethargic bees; the long-term effect is probably to stimulate the recipients to launch into flight. It turns out that the scout bees from the chosen nest site are responsible for producing both the piping signal to prime a swarm for take-off and the buzz-run signal to trigger the take-off. We suggest that these bees produce the signal that triggers take-off because they travel throughout the swarm cluster while piping and so are able to sense when the entire swarm is hot enough to take flight. The mechanisms mediating take-offs by honeybee swarms appear to present us with a rare instance where an action of a large social insect colony is controlled by a small set of individuals that actively monitor the global state of their colony and produce a signal triggering the colony’s action in a timely way. Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Keywords: Apis mellifera; buzz-run; centralized control; group movement; honeybee; ritualization; swarm

Animals that move about in cohesive groups must possess mechanisms of social coordination that enable them to start and stop their movements in unison. In some cases, the mechanism is despotic, that is, one dominant individual decides and directs the others; while in others it is democratic, that is, a majority of group members decide (Conradt & Roper 2003). Examples of species with despotic mechanisms include hamadryas baboons, Papio hamadryas, where the exaggerated swagger of an old male is able to precipitate a band’s morning departure (Kummer 1968), and African elephants, Loxodonta africana, where an adult female will lift one leg and repeatedly

Correspondence: T. D. Seeley, Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, U.S.A. (email: tds5@cornell. edu). 0003e 3472/08/$30.00/0

give long ‘let’s go’ rumbles accompanied by steady ear flapping to incite a stationary group to move off together (Poole et al. 1988). Examples of species with democratic mechanisms include gorillas (Gorilla gorilla), where calling by a majority of a group’s adults signal an impending departure (Stewart & Harcourt 1994), and whooper swans, Cygnus cygnus, where a group takes off when the intensity of head-movement signals reaches a threshold level (Black 1988). Social insect colonies show a high degree of group integration and provide many examples of groups moving as cohesive units (reviewed in Dyer 2000). A vast literature has developed concerning the mechanisms underlying group integration and collective action in social insects (Camazine et al. 2001), but the mechanisms mediating the initiation of their group movements remain poorly studied. Only in the honeybee, Apis mellifera, do we

189 Ó 2007 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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possess some knowledge of how group departures are initiated, specifically, how thousands of bees in a swarm take flight together to fly to their new home. It is known that a swarm of honeybees will hang from a tree branch in a beard-like cluster for several hours or several days while its scouts collectively choose a suitable nesting cavity. This collective decision-making occurs by means of a competition among scouts visiting different prospective nest sites, with each scout tuning the strength of her waggle-dance signals in accordance with nest-site quality, so that the build-up of scout bees occurs most rapidly at the highest-quality site (reviewed in Seeley et al. 2006; Visscher 2007). The selection process ends when the number of scouts at one of the prospective sites exceeds a quorum threshold, indicating that this site has attracted enough attention to be chosen for the swarm’s future home. At this point, the scouts at the chosen site return to the swarm cluster and begin running throughout it while producing high-pitched piping signals, which inform the bees in the swarm cluster to warm their flight muscles in preparation for the flight to their new home (Seeley & Tautz 2001; Visscher & Seeley 2007). After an hour or so of this priming for flight, by which time every bee in the swarm cluster has a thoracic temperature of at least 35 C (Heinrich 1981; Seeley et al. 2003), the bees suddenly launch into flight, form a small cloud of swirling bees and begin moving off together towards their new domicile (described by Beekman et al. 2006). An intriguing mystery is how thousands of bees in a swarm achieve such an explosive take-off. Throughout the warm-up period, one sees that the vast majority of a swarm’s bees (the nonscouts) is quiescent, hanging virtually immobile in the cluster, and that only a small minority (the scouts) are active, running over and burrowing into the cluster. But then, starting about a minute before the take-off begins, one notices that more and more of the surface bees become active, next a few of these bees take flight and finally the whole cluster disintegrates to form a cloud of airborne bees. From start to finish, the process of some 10 000 bees launching into flight typically requires only about 60 s (Seeley et al. 2003). What triggers

the frenzied take-off? The critical releaser may be a threshold level of the Schwirrlauf (hereafter the ‘buzz-run’), an eye-catching behaviour that was first described by Lindauer (1955). Buzz-running bees scramble across the swarm cluster, moving in a zigzag pattern while noisily buzzing their outspread wings, sometimes dashing over the backs of the immobile bees and other times bulldozing between them (Fig. 1). Lindauer (1955) reported that buzz-runners are prominent on the swarm cluster in the final few minutes before take-off starts, and he suggested that by barging and boring their way through the cluster, the buzzrunners disperse the interconnected bees and so initiate their concerted take-off. In this paper, we take up the study of the buzz-run where Lindauer (1955) left it some 50 years ago. In the intervening five decades, only three studies have probed this conspicuous signalling behaviour, perhaps, because it is an ephemeral display that occurs in only a few specific circumstances associated with swarming. Martin (1963) reported its occurrence shortly before a swarm makes its mass exodus from the parental hive, consistent with the hypothesis that its message is ‘Time for departure’. Esch (1967) analysed the sounds produced by buzz-runners and found that the wing-beat frequency within a buzz ranges from 180 to 250 Hz, hence close to that of normal flight. (Note: the fundamental frequencies of piping signals and buzz-runs are the same, but piping signals have strong harmonics and so sound high-pitched whereas buzz-runs lack strong harmonics and therefore sound low-pitched, i.e. buzzy.) And, Mautz et al. (1972) described its use in stimulating swarm bees that are in queenless clusters to take flight and join the queenright cluster nearby, further supporting the view that it is a departure signal. In the present study, we will address the following set of interwoven questions. What is the interplay between worker piping and buzzrunning, as a swarm prepares for and then takes to flight? What is the precise form of the buzz-run? What effect does a buzz-runner have on the inactive bees that she contacts? And which bees in a swarm produce the buzzrun signal?

Figure 1. A worker bee performing the buzz-run. The buzz-runner encounters a small group of lethargic bees that are huddled at the base of the swarm mount when most of the swarm has clustered around the queen near the top of the swarm mount. Panel 1 (left) shows the buzzrunner scrambling over the wooden surface of the swarm mount, approaching in a zigzag run the knot of quiet bees. In panel 2 (1 s later), the buzz-runner first makes contact with the cluster. She has spread her wings and is buzzing them. In panel 3 (1 s after initiating contact), the buzz-runner is pushing through the cluster, still buzzing her wings. In panel 4 (1 s later), she has broken contact with the bees but she continues buzzing her wings as she runs off. The effect of the buzz-runner on the other bees is to disperse them and stimulate them to take flight, thereby hastening their joining of the swarm’s main cluster around the queen. Drawing by Barrett Klein.

RITTSCHOF & SEELEY: HONEY BEE BUZZ-RUN SIGNAL

METHODS

Study Site and Bees All observations were made at the Liddell Field Station of Cornell University, Ithaca, New York (42 260 N, 76 300 W). Because this site is surrounded by woods containing many old trees with cavities, the swarms that we studied had no difficulty in finding suitable nest sites and then flying away. All four swarms studied were artificial swarms prepared from colonies headed by ‘New World Carniolan’ queens purchased from Strachan Apiaries in Yuba City, California. To make each swarm, we first located a colony’s queen and put her in a small wooden cage (1.8  2.9 cm and 8.0 cm high) with wire screen on one side (a standard wooden queen cage). Then, using a large funnel, we shook 1 kg of worker bees (approximately 7500 bees) from the frames of the same colony into a swarm cage (15  25 cm and 35 cm high) made of wood with wire-screen sides. We also placed the caged queen inside the swarm cage. For the next 48e72 h (until copious wax scales appeared beneath the swarm cage), we fed the caged bees ad libitum with a 50% (v/v) sucrose solution. Finally, the swarm cage was opened, the queen (still in her own little cage) was fastened to the swarm mount (described below) and the workers were shaken onto the base of the mount. Within an hour, the workers were clustered over the queen cage and behaving like a natural swarm. After several hours or a few days, the swarm would finish choosing its nest site, take-off and fly away.

Apparatus Swarms were placed on the swarm mount that was described previously (see Fig. 1 in Seeley & Buhrman 1999). The mount consists of a flat vertical board, on which the swarm bees cluster, a post that supports the swarm board and a massive horizontal base. The design of this apparatus facilitates videorecording of the behaviour of workers on the surface of the swarm cluster. Videorecordings were made with a digital video camera (Sony DCR-TRV50) and the recordings were analysed frame-byframe or in slow motion using a video editing deck with variable-speed playback (Sony DSR-30). To evaluate the sounds made by bees running across the surface of the swarm cluster, a small electret condenser microphone (Radio Shack Model 33-3013, 70e16 000 frequency response) was plugged into the video camera and its output was monitored through headphones while being recorded. A 40-mm length of 8 mm internal diameter Tygon tubing was attached to the microphone to make it directional in its sound pickup.

Data Collection and Analysis To measure the rise in number of bees running across a swarm’s surface as it prepared for take-off, we videorecorded a 100  150 mm region (i.e. approximately 50%) of the swarm’s surface starting when the bees began to produce piping signals and continuing to when the swarm

took off. Later, we reviewed the video records and counted the number of bees that ran through the camera’s field of view during the first 15 s of each minute of the 40-min period preceding take-off. While watching the swarm prepare for take-off, we also determined the proportion of the running bees that produced piping signals, buzz-runs, or both, during each 5-min period. We did so by steadily scanning the swarm’s surface for running bees, following each one with the small microphone for at least 5 s, and announcing whether she was piping or buzz-running (or both) for later transcription from the audio track of the videorecording. To obtain close-up videorecordings of buzz-runners to make detailed descriptions of their behaviour, we continued videorecording after the swarm had taken off but we zoomed in the camera’s field of view so that it encompassed just a 28  42 mm area of the wire-mesh screen that covered the front of the cage holding the queen. We had observed that whenever a swarm took off, several agitated worker bees remained on the queen cage where they feverishly produced piping signals and performed buzz-runs, evidently endeavouring to stimulate the queen to take flight. The substrate on which these bees performed their buzz-runs was the 12-mesh hardware cloth of the queen cage, so that their behaviour was automatically recorded against a background grid of lines (wires) spaced 2.1 mm apart. We made video clips of these buzzrunners using iMovie HD and then performed spectrogram analyses of the bees’ buzzing sounds in these video clips using Raven version 1.2.1 (Cornell Laboratory of Ornithology). For each buzz-runner, we measured the fundamental (wing-beat) frequency for at least five bouts of wing buzzing, each of which lasted for at least 0.20 s. We also made videorecordings of bees performing buzzruns in a context other than preparing for take-off, that is, when their swarm was initially getting itself clustered on the swarm mount after it had been shaken from the swarm cage onto the base of the swarm mount. What happens in this situation is that most bees quickly crawl up the mount and cluster on the front side of the vertical board, where they cluster with their queen, but some bees remain behind on the horizontal base of the mount, where they coalesce into flat (monolayer) clusters of two to 10 bees standing quietly together. (Note: small groups of straggler bees are also observed when swarms cluster naturally, and one sees buzz-runners on these straggler groups as well, evidently to get all the swarm bees assembled into one tight cluster.) Buzz-runners intrude upon these peaceful groups, creating commotion. By videorecording the agitated buzz-runners in this context, we measured the effects of their activity on the sluggish bees that they contacted. To measure the effects of buzz-runs on quietly clustered bees, we videorecorded clusters, each containing two to five bees, through which a vigorous buzz-runner ran. We then selected for analysis 20 clusters where the buzzrunner buzzed her wings steadily and performed an action that we will call the ‘wiggle manoeuvre’ (described below) when pushing her way through the knot of bees. From the video records, we measured the mean neighbour distance among the bees in the cluster (not including the

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buzz-runner) at four times: (1) 1 s before the buzz-runner first contacted the cluster; (2) when the buzz-runner first contacted the cluster; (3) 1 s after the buzz-runner first contacted the cluster; and (4) at the end of the buzzrunner’s contact with the cluster (sequence illustrated in Fig. 1). The mean neighbour distance for the group is the mean of the neighbour distances for each of the number of bees in a cluster. Each individual bee’s neighbour distance is her average distance from the n  1 other bees in the cluster. The distance between any two bees was measured as the separation between the midpoints of their bodies, regardless of their orientation to each other. We used the values of mean neighbour distance at the four times to calculate the change in this distance over three time periods for each group that was videorecorded: (1) 1 s before the group was contacted by the buzz-runner; (2) 1 s after the group was contacted by the buzz-runner; and (3) the entire time that the group was contacted by the buzz-runner.

Statistics All descriptive statistics are reported as the mean  1 SD. To test for the equality of two means, we used Student’s t test. To test for the equality of two proportions, we used Student’s t test with an arcsine square-root transformation of the data. For comparing the means of multiple groups in the analysis of the effects of the buzz-run, we used a one-way ANOVA (Sokal & Rohlf 1981) because our measurements had equal variances and normal distributions. When we found a significant difference between groups, we used a post hoc multiple comparisons test to determine which groups were significantly different (Siegel & Castellan 1988), and used a correction of a ¼ 0.05/number of comparisons. To test the significance of regression coefficients, we calculated the standard error of each regression coefficient and tested whether it was significantly different from zero using a t test (Sokal & Rohlf 1981). RESULTS

When Do Buzz-runners Appear on Swarms? In sitting by a swarm and observing the behaviour of the bees on its surface, we saw that, until the last hour or so before the swarm flew away to its new home, the vast majority of the surface bees were essentially motionless and only a small minority were active: crawling about, sometimes producing or following waggle dances and occasionally flying from or returning to the swarm. During the final hour before departure, we began to see bees that were not merely active, but were noticeably excited, for they dashed over the surface of the swarm at high speed (2e6 cm/s; see below). Some of these running bees kept their wings folded tightly over the abdomen and produced high-pitched sounds that lasted for 0.5e1.5 s and had a distinctive upward sweep in frequency. These bees were producing piping signals. Others of the running bees, however, ran about with their wings partially or fully spread, and they vibrated their wings, producing

low-pitched, monotonic, buzzy sounds. These bees were performing buzz-runs. And, still others of these excited running bees produced both piping signals and buzz-runs. To see how the numbers of pipers and buzz-runners changed as a swarm prepared for departure, we videorecorded a portion of the surface of a swarm to measure the incidence of the high-speed runners, and at the same time we scanned the swarm’s entire surface for runners and listened to each one individually with a small microphone to determine what signal(s) she was producing. This protocol was applied to two swarms and the results are shown in Figs 2 and 3. We see that in both swarms, there was a steep and steady rise in the number of running bees during the final 40-min period preceding take-off (Swarm 1: slope of the regression line ¼ 0.19 additional runners/min, t test: t6 ¼ 5.75, P < 0.005; Swarm 2: slope of the regression line ¼ 0.20 additional runners/min, t test: t6 ¼ 4.25, P < 0.01). We also see something even more remarkable: all of the running bees were producing audible signals, that is, pipes or buzzes, or both. Furthermore, over the final 40 min, there was a dramatic shift in the proportions of the two types of signals produced by the running bees. Initially, they produced almost exclusively piping signals, but gradually they increased their wing buzzing so that during the final 5 min before takeoff, more than 80% of these excited bees produced buzzruns. Indeed, in the final 5-min time block, nearly onethird of the running bees performed buzz-runs exclusively.

What is the Precise Form of the Buzz-run? The buzz-runners that we observed were highly agitated bees that scrambled about turning this way and that, usually with their wings whirring, sometimes butting through knots of bees and other times executing yet another movement, a conspicuous wiggling action of the entire body. Confronted with such behavioural complexity in these hyperactive bees, we needed to videorecord them and analyse the recordings in slow motion to visualize clearly their movement patterns. We found that the best opportunity for filming buzz-runners came after a swarm had taken off, at which time only a handful of worker bees remained on the swarm mount. These few bees frantically performed worker piping and buzzrunning on the vertical front side of the cage holding the queen, and this provided us with an opportunity for videorecording bees performing buzz-runs within a small area, hence one that favoured close-up videography. We performed a frame-by-frame analysis of the video records of 10 different bees, each of which performed buzz-runs as she ran excitedly about on the queen cage. These bees were tracked for 5.2  0.9 s; longer trackings were not possible because these storming bees ran in and out of the camera’s field of view. Figure 4 depicts the travel pattern of one typical buzz-runner. As 10 buzz-runners scurried about in a zigzag fashion, they ran at a speed of 4.2  0.8 cm/s and they buzzed their wings 91  13% of the time. Their wing-beat frequency while buzzing was 204  16 Hz. While running and buzzing, they sometimes butted headfirst against other bees for a fraction of a second (0.25  0.16 s, N ¼ 28 butting

RITTSCHOF & SEELEY: HONEY BEE BUZZ-RUN SIGNAL

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Minutes before start of take-off Figure 2. Records for two swarms of the increase in number of bees running over the surface of a swarm cluster during the 40-min period preceding swarm take-off. Each bar indicates the mean count of bees that ran through a 100  150 mm region of the swarm’s surface in 15 s. For each 5-min interval, five counts were made.

episodes for all 10 bees), so that 14  10% of each buzzrunner’s time was devoted to butting other bees. Other times, they added to their running and buzzing actions, a curious wiggling manoeuvre which involved executing a fluid series of small but rapid body rotations, alternately left and right, while running steadily along. The net result was a sinuous motion (see Fig. 4) that usually lasted for only a fraction of a second (0.32  0.25 s, N ¼ 23 wiggling episodes for all 10 bees). On average, the buzz-runners devoted 15  5% of their time to wiggling, similar to the 14  10% that they devoted to butting. Unlike in butting, however, wiggling did not always involve contact between

the buzz-runner and another bee; only 14 of the 23 episodes of wiggling occurred when the buzz-runner was pushing against other bees. Ten buzz-runners just described appeared to be exceptionally motivated signallers, for these bees buzzed their wings almost continuously as they scrambled over the queen cage in great excitement. In comparison, when we watched bees producing buzz-runs among idle bees that were lingering in small, queenless clusters at the base of the swarm mount, presumably to stimulate them to join the main, queenright cluster atop the swarm mount, we noticed that these buzz-runners buzzed their wings only

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Minutes before start of take-off Figure 3. The changing pattern of signal production by the bees running over the surface of a swarm cluster, during the 40-min period preceding swarm take-off. During each 5-min interval for both swarms, 12.8  1.2 runners were followed and monitored acoustically for at least 5 s each. All running bees produced pipes or buzzes, or both.

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Figure 4. (a) Travel pattern, from a videorecording, of one worker bee producing the buzz-run signal as she ran over the front of the cage holding the swarm’s queen after the rest of the swarm had departed. This record depicts a 5.6-s segment of her activity; numbers and dots along her track denote 1- and 0.1-s intervals, respectively. (b) Detailed view of the body movements made by the buzz-runner when she produced a 0.4-s bout of the wiggling manoeuvre starting at the 3.1-s mark in the record shown in the top panel. The bee was videorecorded at 30 frames/s, so the entire manoeuvre comprised 13 frames. Between frames, the bee rotated her body axis by 25  13 , alternating between clockwise and anticlockwise turns, and moved forward by 2.5  0.8 mm, thereby generating a conspicuous sinusoidal movement.

intermittently. We videorecorded 30 of these less energetic buzz-runners, tracking each bee for 5.6  3.6 s before losing her, usually when she took flight (22 of the 30 trackings ended when the buzz-runner took flight). Analysis of the videorecordings revealed that these bees ran with a mean speed of 3.6  1.4 cm/s, not significantly different from that of the buzz-runners described above (two-sided t test: t38 ¼ 1.00, P > 0.25), but that they buzzed their wings only 55  28% of the time, significantly less than the previously described buzz-runners (two-sided t test: t38 ¼ 3.72, P < 0.001). Moreover, they mainly produced short bursts of wing buzzing, each one lasting for only 0.34  0.23 s (N ¼ 114 bouts of less than 1 s), though occasionally they produced persistent periods of wing buzzing, each one lasting for 1.85  0.83 s (N ¼ 22 bouts of 1 s or more). When they produced extremely brief buzzes, some of which were mere flits of the wings lasting for just 0.03e0.06 s (one to two video frames), these bees often spread their wings only partially, as if they were not fully motivated to produce the buzz-run signal.

Figure 5. Change in tightness of clusters of bees during the second before and the second after each cluster was initially contacted by a buzz-runner, and during the entire period that a buzz-runner contacted each cluster. Letters above bars indicate which groups had significantly different (P < 0.05) values for the change in mean neighbour distance.

What Effect Does a Buzz-runner Have? It seemed to us that after a buzz-runner had pushed through a knot of largely motionless bees, these bees were somewhat dispersed and activated. We checked this impression by videorecording 20 small clusters of bees lingering on the base of the swarm mount when most of a swarm’s bees were clustered around the queen at the top of the swarm mount. We then analysed the videorecordings to see how the separation of the clustered bees changed before and after a buzz-runner barged through them. In each case, the buzz-runner buzzed her wings and performed the wiggle manoeuvre when pushing her way through the knot of lethargic bees. Figure 1 shows a specific case and Fig. 5 shows the general results. During the 1 s before being contacted by a buzz-runner, on average, the group members clustered themselves a bit more tightly (mean neighbour distance decreased by 1.13 mm). During the next second, however, when the buzz-runner plowed through the cluster, they separated from one another by nearly a full bee length (mean neighbour distance increased by 11.65 mm). By the time the buzz-runner broke contact with each cluster, the bees were even more dispersed than after 1 s of buzz-runner influence, though not significantly so. The passage of the buzzrunner through the clustered bees significantly affected their separation (ANOVA: F2,57 ¼ 50.58, P < 0.02). Also, the bees contacted by a buzz-runner became noticeably more active under the influence of the buzz-runner, but

RITTSCHOF & SEELEY: HONEY BEE BUZZ-RUN SIGNAL

none took flight within the period of videorecording of each cluster (6e14 s).

DISCUSSION When the honeybee’s buzz-run (Schwirrlauf ) was first reported by Lindauer (1955) more than 50 years ago, he provided the following description: In performing [the buzz-run], the participating bees, which are highly excited and nervous, force themselves through other bees that are standing around. They also vigorously shove other bees aside while making disorderly zigzag runs, during which they strongly vibrate the abdomen and furthermore produce clearly audible wing buzzings. (page 315; translation by T.D.S.) Now, having closely examined the form of this behaviour, we can confirm Lindauer’s description and can provide some additional details. Certainly, the behaviour is aptly named, for buzz-runners do indeed buzz their wings and they do indeed run, generally tracing out crooked, twisty paths of travel. We found, however, that the wing buzzing activity is often discontinuous, consisting of a string of short bursts of buzzing, sometimes mere flits of the wings. Also, we found that not all the bees that are running zigzag across the surface of a swarm are buzz-runners, for many are producing the wings-together form of worker piping (Seeley & Tautz 2001), especially during the early stages of a swarm’s preparations for take-off. As for Lindauer’s report that buzz-runners ‘vigorously shove other bees aside’ and ‘strongly vibrate the abdomen’, this certainly matches what we observed, and we can add that the pushing of other bees aside by buzz-runners tends to occur sporadically, in brief episodes (<0.5 s), as does the vibrating of the buzz-runner’s abdomen. The latter action, as revealed by slow-motion video analysis, is actually better described as a winding or sinusoidal movement of the buzz-runners’ entire body, not just a vibrating of her abdomen, as she snakes her way forward, often while pushing through a clump of inactive bees. One feature of the buzz-run behaviour that Lindauer does not mention is that it often ends with the signalling bee launching herself into flight, flying for a few seconds around the swarm cluster, and then landing on it to continue her buzz-running. This point is important because it is likely that the buzz-run signal is a ritualized form of a bee’s take-off behaviour: she spreads her wings, activates them with a wing-beat frequency of approximately 225 Hz, pushes clear of other bees if need be, and takes to the air (Sotavalta 1947). It is generally recognized that ritualization, the process of signal evolution whereby an incidental cue becomes an intentional signal (Bradbury & Vehrencamp 1998), has played an important role in the evolution of communication signals in social insects (Ho¨lldobler 1984). The honeybee’s buzz-run, however, reveals especially clearly the evolutionary origins and ritualization process of a signal. In the process of signal evolution, the critical first step is the establishment of an association between a particular condition of the

sender and the production of some cue (structure, movement, sound or chemical) by the sender (Otte 1974). Often this association arises if the cue is an inevitable by-product of an activity performed in a particular context. The buzz-run illustrates this idea nicely: whenever a bee embarks on a flight, she inevitably buzzes her wings. The critical second step in the signal evolution is for potential receivers to detect the cue and to use its occurrence to improve their decision-making. If the improvement in the receivers’ decision-making also boosts the fitness of the senders, then there will be feedback on the senders to improve the detectability and information content of the cue. In the case of the buzz-run, the quiescent bees in a swarm were probably preadapted to detect the cue of wing buzzing, by already possessing the sensory capacities to detect the buzzing visually or mechanically (as an airborne sound or a tactile vibration, or both), and in doing so, they probably improved their decision-making about when to initiate flight. Their improved decisionmaking no doubt gave rise to better synchronized and thus more efficient take-offs, which boosted the fitness of the senders, hence there was a positive feedback on the senders favouring modifications of the cue of wing buzzing to increase its signal value to the quiescent bees. Given the present-day form of the buzz-run, it appears that these modifications include: (1) ‘exaggerating the cue’ by greatly increasing the buzzing duration so that it no longer occurs just immediately before taking flight; (2) ‘simplifying the cue’ by lowering the wing-beat frequency below that for flight; and (3) ‘adding behavioural elements to the cue’ such as running, butting, and wiggling. Following the terminology of Tinbergen (1952), the evolution of the buzz-run signal also appears to have involved ‘emancipation’, for the production of this signal is no longer tightly coupled to the internal and external factors that originally triggered wing buzzing for flight. Many bees begin producing buzz-runs long before they launch into flight. Besides clarifying the form and evolutionary origins of the buzz-run signal, this study has helped solve the mystery of who produces the buzz-run signal. The present study has provided one essential clue: ‘the buzz-runners are the same bees as the pipers’. All pipers run across the surface of their swarm, and our analysis of the bees running on two swarms revealed that these runners start out producing mostly piping signals, then they produce both piping and buzzrun signals, and shortly before take-off they often produce only buzz-runs. Another study (Visscher & Seeley 2007) has provided the second crucial clue: ‘the pipers are exclusively nest-site scouts, and probably only those that are affiliated with the chosen site’. Therefore, given that pipers are nestsite scouts, and given that pipers (i.e. running bees) become buzz-runners, we deduce that buzz-runners are also nestsite scouts, and probably only those from the chosen site. Evidently, these particular bees give both the piping signal to prime the swarm for take-off and the buzz-run signal to trigger the take-off. Although we believe that the effect of the buzz-run signal is to stimulate bees to take flight, we did not succeed fully in demonstrating this effect. We showed that when a buzz-runner barges her way through a group of inactive

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bees, she has an immediate effect of dispersing them and stimulating them to become active. Future work, however, needs to follow the bees contacted by buzz-runners for several minutes, not just a few seconds, to test more thoroughly the hypothesis that receiving the buzz-run signal raises a bee’s probability of launching herself into flight. At this point, the strongest evidence that the buzz-run signal stimulates swarm bees to take flight is that its production crescendos moments before a swarm takes flight. There is also the reality that the context in which the buzz-run signal is produced is consistently one in which idle bees are being stimulated to take flight (cf. Martin 1963; Mautz et al. 1972). Our final point of discussion is the question of why honeybees have evolved this buzz-run signalling system, whereby the scout bees from the chosen site evidently inform the other bees in the swarm when to launch into flight. We suggest that this signalling system evolved because it is only the highly mobile scout bees that are able to sense when all the bees in the swarm cluster are ready for departure, and a special signal enables them to share this crucial piece of information. Readiness for flight to the new home depends critically on all the bees in the swarm having a thoracic temperature of at least 35 C, which is needed for rapid flight (Heinrich 1981). Indeed, it is not until 100% of the coolest, outermost bees in a swarm cluster have achieved this temperature that the swarm takes off (Seeley et al. 2003). How can ‘all’ the bees in a swarm know when they are ‘all’ hot enough? One way would be to have some bees travel all about the cluster, census the temperatures of their swarm mates, integrate this information to determine the global temperature state of the swarm, and produce a departure signal when their polling has revealed that the required warmth has been achieved. It seems likely that this is how it works on swarms, for we now know that the scouts from the chosen site move quickly throughout the swarm cluster, with each one pausing every few seconds to press her thorax against another bee and produce the piping signal that stimulates warming (Seeley & Tautz 2001; Visscher & Seeley 2007). And, we now know that it is these same bees that strongly produce the buzz-run signal in the final few minutes before take-off, when all the bees are reaching the high body temperature required for departure. If the idea just presented proves correct, then the mechanisms mediating the initiation of take-offs by honeybee swarms present us with an intriguing system of control within a social insect colony, one in which a small subset of individuals actively census the entire colony to collect information about its global state and then, when the colony reaches a critical state, they produce a signal that triggers an appropriate action by the whole colony. Such a control system would not be unusual in species with small (<100 member) colonies, where the queen can accurately monitor the conditions colony-wide and can function as a central pacemaker of colony activities (e.g. Reeve & Gamboa 1983, 1987; but see Jha et al. 2006). In species with large colonies, however, it is widely understood that there is little if any central control and that each individual responds to local information from other workers or from the nest in a manner that meets the needs of the colony (reviewed in

Anderson & McShea 2001; Camazine et al. 2001; Jeanne 2003). Important exceptions to this general pattern may exist, however. Besides the possible exception reported here ¨ lldobler (personal communicainvolving honeybees, Ho tion) has reported that during the display tournaments of the honey ant, Myrmecocystus mimicus (Ho¨lldobler 1981; ¨ lldobler 1983), some workers from each colLumsden & Ho ony move rapidly among the displaying ants, apparently conducting large-scale sampling to assess the relative strengths of the two colonies and producing recruitment signals to restore the balance of power when necessary. Future studies are needed to check the intriguing possibility that there are times when a small minority of the workers in a large social insect colony monitor the overall state of their colony and provide centralized control of certain of its actions.

Acknowledgments We thank the Hughes Summer Scholars Programme at Cornell and the National Science Foundation (grant IBN02-10541) for financial support, Barrett Klein for the drawing of a buzz-runner and Heather Mattila forconstructive comments on the manuscript. This paper is based on the undergraduate honours thesis of C.C.R.

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