Apidologie 35 (2004) 117–131 © INRA/DIB-AGIB/ EDP Sciences, 2004 117 DOI: 10.1051/apido:2004006 Review article

The vibration signal, modulatory communication and the organization of labor in honey , Apis mellifera

Stanley S. SCHNEIDER*, Lee A. LEWIS

Department of Biology, University of North Carolina, Charlotte, NC 28223, USA

(Received 10 July 2003; revised 17 October 2003; accepted 15 December 2003)

Abstract – Cooperative activities in honey colonies involve the coordinated interactions of multiple workers that perform different, but interrelated tasks. A central objective in the study of sociality therefore is to understand the communication signals used to integrate behavior within and among worker groups. This paper focuses on the role of the “vibration signal” in organizing labor in honey bee colonies. The vibration signal functions as a type of “modulatory communication signal”. It is directed toward diverse recipients, causes a non-specific increase in activity that may alter responsiveness to a wide array of stimuli, and thus may influence the performance of many different tasks simultaneously. We review the empirical evidence that the signal is involved in coordinating at least three colony-level activities: food collection and foraging-dependent tasks, queen behavior during and queen replacement, and house hunting by honey bee swarms. Signals that function like the vibration signal may be widespread in highly social insects and social animals in general, and may help to fine-tune the collective decision-making processes that underlie cooperative actions in a wide array of species. vibration signal / modulatory communication / collective decision making / Apis mellifera / multimodal signals

1. INTRODUCTION At the heart of cooperative behavior in many social insects is a complex system of Cooperative efforts in social insects are communication signals that influence worker often regulated by collective decisions that task performance. These signals can be emerge through decentralized systems of divided into two main categories based on how control (Seeley, 1995; Beshers et al., 1999; they influence worker behavior. The first cate- Camazine et al., 2001). Many colony activities gory includes signals, such as the waggle require the interaction of multiple worker dance, tremble dance and grooming dance of groups that perform interrelated tasks, but honey bees, which are produced in specific which respond to different stimuli, attend to contexts, influence only certain workers and different aspects of the colony environment, elicit specific responses. These signals help to and may be congregated in different regions of organize one or a few specific tasks within the nest. A central challenge in the study of particular groups of workers, most of which insect sociality, therefore, is to understand the respond to the same stimuli. But, how is activ- mechanisms used to organize information ity coordinated among different worker flow and integrate labor within and among groups, which often attend to different sets of worker groups, so that a colony functions as a stimuli? Such coordination may be governed coherent whole. in part by a second category of signals,

* Corresponding author: [email protected] 118 S.S. Schneider, L.A. Lewis referred to as “modulatory signals” (Markl, “shaking”, the “shaking dance”, and the “jerk- 1985). These signals are produced in a variety ing dance”, (Rütteltanz: from the German rüt- of contexts and elicit nonspecific effects that teln, to jiggle, shake or vibrate) (Schick, 1953; shift slightly the probability of engaging in Allen, 1958, 1959a, b; Gahl, 1975; von Frisch, other behavioral acts (Hölldobler and Wilson, 1967), the “trembling movement” or “vibra- 1990). Because of their generalized manner of tion movement” (Zitterbewegung: from zit- operation, modulatory signals can influence tern, to shiver, tremble or vibrate) (Hammann, many different workers and alter the perform- 1957), the “vibratory dance” (von Frisch, ance of many different activities simultane- 1967; Fletcher, 1978a, b; Bruinsma et al., ously. Modulatory signals may therefore be an 1981), the “vibration dance” (Schneider, 1986, important component in the organization of 1987, 1989; Schneider et al., 1986a, b); the labor in honey bees, and social insects in gen- “shaking signal” (Seeley et al., 1998; Nieh, eral (Hölldobler and Wilson, 1990; Beshers 1998; Biesmeijer, 2003), and the “vibration et al., 1999; Hölldobler, 1999). However, signal” (Painter-Kurt and Schneider, 1998a, b; compared to our knowledge of specific-func- Visscher et al., 1999; Lewis et al., 2002; Lewis tioning signals, our understanding of modula- and Schneider, 2000; Donahoe et al., 2003; tory signals is rudimentary. Schneider and Lewis, 2003). Von Frisch An example of a modulatory signal is the (1967) and Fletcher (1978a) cautioned against vibration signal of the honey bee, which con- the use of the “shaking” nomenclature, noting sists of a worker rapidly vibrating her body that this created confusion because “shaking” dorso-ventrally for 1–2 s, usually while grasp- had already been identified as a synonym for ing a recipient with her forelegs. Vibrating the grooming dance. In the earlier literature, bees typically roam over large areas of the nest the most commonly used name was the and produce series of signals (up to 20 or more D-VAV. However, this is an inaccurate acro- per min) that last from several minutes to over nym, because it is not only the abdomen that is an hour (Schneider, 1986; Nieh, 1998; Lewis vibrated (Visscher et al., 1999). In addition, et al., 2002; Schneider and Lewis, 2003). The the behavior does not involve the complex vibration signal is one of the most commonly motions of honey bee “dances” and is more occurring communication signals in honey bee appropriately referred to as a signal. There- colonies and is performed on many different fore, we use the term “vibration signal”, recipients, including workers of all ages, lay- because it accurately describes the tightly con- ing queens, virgin queens and developing trolled, up-and-down motions produced and queen cells (Painter-Kurt and Schneider, clearly distinguishes the signal from the more 1998a, b). It causes a general increase in activ- “shaking-like” and “trembling-like” signals ity that influences a wide array of cooperative such as the grooming dance and tremble interactions, including foraging, brood care, dance. queen rearing, colony reproduction and swarm The purpose of this review is to summarize movements (Schneider and Lewis, 2003). The the existing information on the vibration sig- signal is therefore used in many different nal and examine its role in cooperative activi- contexts and may have a broad utility in ties of honey bees. Our review has three main colony life. goals. First, we explore the modulatory nature However, controversy has surrounded the of the signal by examining: (1) the workers function of the vibration signal and we have that perform vibration signals and the factors only recently begun to understand its role in associated with signal production, (2) the honey bee social behavior. Indeed, even the recipients of vibration signals and the name of the signal has been the subject of responses elicited, and (3) the possible mes- debate. Over the years, it has been referred to sage and meaning of the signal. Second, we as the “joy dance”, “good-time dance” and the examine how the signal may help to organize “dance of contentment” (Haydak, 1929, three cooperative interactions: food collection 1945), the “spirit-tap dance” and “pep-tap and foraging-dependent tasks, colony repro- dance” (Milum, 1955), the “dorso-ventral duction and queen replacement, and house abdominal vibration” or “D-VAV” (Milum, hunting by swarms. Finally, we address the 1955; von Frisch, 1967; Fletcher, 1975), possible role of modulatory communication in Vibration signal and modulatory communication 119 collective decision making in honey bee soci- behavior (Bruinsma et al., 1981; Fletcher, eties, and social systems in general. 1978a) and may also be associated with some aspects of queen pupal development (Schneider and DeGrandi-Hoffman, 2002; see 2. THE MODULATORY NATURE Sect. 3.2). OF THE VIBRATION SIGNAL Thus, vibration signals are produced by a small proportion of workers in response to 2.1. Signalers and the factors associated different stimuli, depending upon signaler age with vibration signal performance and contextual cues. The generalized nature of Studies that have monitored marked bees vibration signal performance may therefore have revealed that, on average, only about allow this one signal to influence many 13% of workers ever perform vibration signals different cooperative activities in honey bees. during their life times (Painter-Kurt and Schneider, 1998a, b). However, within this 2.2. Recipients of the signal subset of workers, signal production is not and the responses elicited restricted to particular age groups. The major- ity of vibration signals are produced by older Vibration signals are focused on certain workers of foraging age (Gahl, 1975; Painter- recipients that are chosen from an array of Kurt and Schneider, 1998a, b). Nevertheless, potential receivers. As a vibrating bee roams workers of all ages greater than two days old throughout the nest, she contacts hundreds of have been observed to perform vibration sig- different workers of all ages that are engaged nals on workers, queens and queen cells in many different activities (Gahl, 1975; (Allen, 1959a; Gahl, 1975; Painter-Kurt and Schneider, 1985, 1986; Nieh, 1998; Lewis Schneider, 1998a, b). et al., 2002). However, less than half of these The broad age range of vibrating bees sug- bees receive vibration signals, while the gests that signaling activity is not associated remainder are “bypassed” (antennated but not with any particular aspect of colony labor and, vibrated; Lewis et al., 2002). Recipients are indeed, a wide variety of factors may influence not selected based on age or relatedness, nor signal production. Many of the vibration is signaling activity directed preferentially signals performed on workers are produced by toward bees associated with certain tasks foragers, and foraging success may be the (Lewis et al., 2002). Rather, the likelihood of a primarily factor that stimulates signaling worker receiving vibration signals may be behavior by older bees (Schneider, 1986; influenced by her activity level. Both active Painter-Kurt and Schneider, 1998a; Seeley and inactive bees can be vibrated; however, et al., 1998; Nieh, 1998; Biesmeijer, 2003). there is a slight, but significant tendency to However, 10–20% of the total signalers in a direct signaling activity toward less active colony are young bees that have no observable workers of all ages (Lewis et al., 2002). association with food collection or foraging- Workers respond to the vibration signal related tasks (Painter-Kurt and Schneider with increased activity (Schneider and Lewis 1998a). About a third of these young vibrators 2003). This change in behavior is not immedi- perform signals during periods of orientation ate and often does not become detectable until flight (Painter-Kurt and Schneider, 1998a; 15–30 min after the signal has been received Biesmeijer, 2003), which suggests that signals (Schneider et al., 1986a; Schneider, 1987; performed on workers may be triggered by dif- Schneider and McNally, 1991; Nieh, 1998). ferent stimuli in different signaler age groups. The effect of the signal is most often expressed Furthermore, vibration signals can also be pro- as heightened locomotion (Schneider et al., duced in response to queen behavior. Signals 1986a; Nieh, 1998), but is also manifested as may be triggered by queen activity level, greater task performance (Schneider, 1987; because both laying queens and virgin queens Schneider and McNally, 1991). The specific receive more vibration signals when inactive tasks performed depend in part upon a recipi- than active (Schneider, 1990; but see Fletcher, ent’s age. Foraging-age recipients respond by 1978a). Signals performed on queens cells moving to the “dance area” near the entrance may be influenced by queen emergence of the nest, where they have an increased 120 S.S. Schneider, L.A. Lewis likelihood of contacting the waggle dances 2.3. The message and meaning and odor cues that recruit them to food sites of the vibration signal (Schneider et al., 1986a; Nieh, 1998). In con- trast, younger workers respond with increased Given the variability in the age of vibrators time spent in in-hive tasks, such as brood care, and recipients, the different stimuli associated food processing, and comb manipulation with signal performance, the wide range of (Schneider, 1987; Schneider and McNally, responses elicited, and the many contexts in 1991). which the signal is used, it has been unusually difficult to determine the message conveyed The vibration signal may influence worker by signalers and the meaning of the vibration behavior by affecting response thresholds. The signal to receivers. Allen (1958) suggested heightened locomotion elicited by the signal that the message was “prepare for flight”, could increase contact with other signals and cues, so that a recipient more quickly based on her observations that queens receive reaches the threshold for triggering a specific vibration signals only during the periods that response. Additionally, the signal could lower precede swarming or mating flights. In con- response thresholds so that less stimulation is trast, Fletcher (1975, 1978a, b), who also mon- required to activate the performance of a par- itored signals performed on queens, proposed ticular task. The juvenile hormone (JH) titers an opposite message for the vibration signal, of workers 15–30 min after receiving vibration namely “reduce your activity”. However, sub- signals are slightly, but significantly higher sequent work has suggested that vibration sig- than those of non-vibrated control bees that nals are associated with increased activity in are matched for age, location in the nest and all recipients, including queens (Schneider, initial activity levels (Schneider, Huang and 1991), which led Seeley et al. (1998) to pro- Lewis; unpublished data). The function of the pose the general message “prepare for greater increased JH titers is unknown. However, JH activity”. Nieh (1998) suggested that the sig- contributes to the changing response thresh- nal conveys the message “reallocate labor for olds associated with the age-based division of different activities or activity levels”, based on labor in honey bees, and may also affect observations that (1) vibrated workers can behavior on more short-term time scales increase the number of tasks performed (Huang and Robinson, 1999; Elekonich et al., (Schneider, 1987; Schneider and McNally, 2001). This raises the possibility that the 1991) and (2) vibration activity often increases delayed, non-specific influence of the vibra- at the end of the day when foraging is ceasing, tion signal may arise from a physiological but tasks such as food processing and brood effect that could potentially alter responsive- rearing must continue (Nieh, 1998). In a simi- ness to a wide array of stimuli. This, in turn, lar vein, Biesmeijer (2003) suggested that the could facilitate the integration of multiple message of the signal is, “reassess your current stimuli and result in more fine-tuned decisions activity”, based in part on the variability in by individual bees (Nieh, 1998). Thus, in for- recipients’ responses. However, the latter two aging-age recipients the vibration signal may proposed messages may be unnecessarily interact with waggle dances, tremble dances complicated. While recipients have an and odor cues to help formulate specific deci- increased likelihood of switching tasks, they sions about food gathering. In younger work- can respond by increasing the time spent per- ers, the signal may work in conjunction with forming one task (Schneider, 1987; Schneider brood pheromones, cues emanating from food and McNally, 1991). Thus, there is not an comb, and interactions with other bees to inevitable reallocation of effort to different determine responses consistent with an indi- activities. Likewise, the variability in worker vidual’s age and physiological state. By being responses does not necessarily indicate a performed on bees of all ages and influencing broad-based reassessment of activity budgets, response thresholds, the vibration signal can but rather may simply reflect the strong role of affect many different activities simultaneously contextual cues in determining a worker’s and may help to organize information flow ultimate reaction. among worker groups that perform interre- Therefore, we propose that the message lated tasks. of the vibration signal is, “increase your Vibration signal and modulatory communication 121 activity”, with the specific response of a recip- requires the integration of numerous worker ient being idiosyncratic and arising from an groups, and the degree to which this interaction of her age, physiological condition, occurs may need to vary with changes in the genetically influenced response thresholds, foraging environment and colony require- work history and the other stimuli impinging ments (Winston, 1987; Seeley, 1995). One of on her at the time the signal is received. Thus, the main functions of the vibration signal may inactive recipients may respond by becoming be to facilitate the behavioral integration nec- active, whereas already-active recipients may essary to balance colony labor with resource become more active. Some recipients may abundance. respond with only increased locomotion, some Many vibrating bees show an immediate may increase their performance of one partic- association with food collection and, on aver- ular task, others may switch to different tasks, age, 10–25% intermix signaling activity while still others may exhibit no observable with waggle dances and tremble dances, or change in behavior if contextual cues do not perform vibration signals while carrying pol- trigger specific acts. In this manner, the same len loads (Schneider, 1986, 1989; Schneider signal with a general message can be directed and McNally, 1991; Nieh, 1998; Painter-Kurt toward many recipients in a variety of contexts and Schneider, 1998a; Seeley et al., 1998; and have different specific meanings that gen- Biesmeijer, 2003). Several aspects of foraging erate an array of particular responses. How- have been suggested to contribute to signal ever, the exact mode of operation of the vibra- performance, including: (1) the resumption tion signal remains unclear and definite of food collection after a period of dearth conclusions must await a more complete (Schneider et al., 1986b; Seeley et al., 1998); understanding of the physiological effects (2) contacting and following waggle dancers elicited by the signal. Nevertheless, the avail- (Biesmeijer, 2003); (3) changing colony nutri- able evidence suggests that the modulatory tional needs (Schneider et al., 1986b); (4) nature of the vibration signal makes it espe- higher quality food sources (Painter-Kurt cially well suited to influence multiple tasks and Schneider, 1998a); and (5) temporal pat- simultaneously, and thus to help integrate the terns of forage availability (Schneider et al., actions of individual workers into colony- 1986a, b). level behavior patterns. Daily patterns of colony-level vibration activity often show a distinct rhythm that is 3. ROLE OF THE VIBRATION associated with changes in foraging success SIGNAL IN ORGANIZING (Fig. 1). Small, “minor peaks” of vibration COLONY ACTIVITIES activity occur throughout the afternoon hours and often coincide with increases in waggle 3.1. Food collection dance behavior. Large, “major peaks” of and foraging-dependent tasks vibration signaling occur in the early morning and can precede the onset of foraging by sev- Much of the vibration signal activity that eral hours (Fig. 1) (Schneider, 1986a, b; Nieh, occurs between workers may help to synchro- 1998; Biesmeijer, 2003; Schneider and Lewis, nize foraging and related tasks. Many of the 2003). Schneider et al. (1986b) demonstrated activities performed by individual workers experimentally that major morning vibration must be adjusted to the availability of food in peaks are abolished if colonies are prevented the nest and in the field. For example, brood from foraging for 2–4 days, but are reinstated rearing, food processing and comb construc- following 3–4 consecutive days of high levels tion are performed by different groups of of food intake. Many of the signals performed young and middle-aged workers and are during morning peaks are produced by forag- dependent upon the rate at which pollen and ers that were successful on previous days nectar are harvested and stored in the hive. (Schneider et al., 1986b; Biesmeijer, 2003). These tasks, in turn, influence the foraging Furthermore, there is a significant, positive activity of older workers and the types of relationship between the amount of vibration resources they gather. Coordinating food col- signaling in the early morning hours and the lection and foraging-dependent tasks therefore level of waggle dance activity occurring later 122 S.S. Schneider, L.A. Lewis

ioral integration. Indeed, Nieh (1998) sug- gested that the daily pattern of vibration activity operates as a “work whistle”, with major morning peaks activating foraging and associated tasks at the beginning of the day and evening peaks directing labor more toward in-hive activities at the end of the day. Thus, by responding to foraging success and promoting task performance in different worker groups, the vibration signal may help to adjust numerous aspects of colony labor Figure 1. Representative daily patterns of vibration signal and waggle dance activity in a honey bee with both short- and long-term trends in colony. Signaling activity is typically characterized resource abundance. by small “minor” peaks which occur throughout the afternoon hours and often coincide with increased waggle dance activity. Large “major” vibration peaks occur in the early morning and often precede 3.2. Colony reproduction and queen foraging by several hours. An evening peak of replacement vibration signal activity can also occur at the end of the day when foraging is ceasing. While vibration signals are most commonly directed toward workers, they can also be per- formed on laying queens (LQs), virgin queens that same day (Schneider et al., 1986a). Major (VQs) and queen cells. However, queens are morning vibration peaks may therefore be vibrated only in association with reproductive based on the foraging success experienced swarming and queen replacement. During over several preceding days and help to adjust swarming, the LQ must leave the natal nest foraging activity for the upcoming day accord- with about half of the workers and relocate to ingly. Increased vibration activity can also a new nest cavity. Simultaneously, VQs must occur in the evening as foraging is ending be produced in the parental nest to replace the (Fig. 1) (Schneider et al., 1986a; Nieh, 1998; mother queen. Queen replacement also occurs Biesmeijer, 2003). There is a positive correla- when a failing queen is superceded and in tion between the height of the major morning “emergencies” when a laying queen is lost. All vibration peak and the level of evening vibra- instances of queen replacement consist of two tion activity occurring on the same day (Nieh, distinct phases: (1) ‘queen rearing’, in which 1998), which suggests that evening vibration VQs are raised in specially constructed queen activity may also be associated with the forag- cells, and (2) ‘queen elimination’, in which the ing success experienced over an extended number of VQs remaining in the nest is period of time. reduced to one (reviewed in Tarpy et al., 2004; Thus, daily patterns of vibration signal Tarpy and Gilley, 2004). Some emerged VQs activity may help to adjust foraging and forag- may depart in secondary swarms, called after- ing-dependent tasks on two times scales. swarms (Winston, 1987). More typically, Minor vibration peaks may function to adjust however, VQs attempt to destroy unemerged food collection and related activities to short- “rivals” in queen cells and battle other term changes in foraging success. In contrast, emerged queens to the death (Gilley, 2001). major morning peaks may prime the work- The end result is a sole surviving VQ that takes force for the upcoming day’s labor relative to mating flights and becomes the new laying long-term trends in food availability. During queen of the natal nest. Thus, to a large extent, sustained periods of floral abundance, tasks the reproduction and continued survival of such as pollen and nectar collection, food honey bee colonies depends upon queen processing, comb construction and brood rear- behavior. The vibration signal may be one ing may all need to be increased simultane- mechanism used by workers to help to ously and in a balanced manner. Increased adjust queen activity to the different aspects morning vibration activity during these peri- of the reproductive and queen replacement ods could help to achieve this level of behav- processes. Vibration signal and modulatory communication 123

will lead to departure with swarms (Schneider, 1991; Nieh, 1998). The signal may also help to regulate egg laying during the swarming period. Egg production and ovarian develop- ment must decline for LQs to achieve flight. However, some oviposition must continue to maintain the worker population in the nest after the queen leaves and allow the rapid resumption of egg laying once the swarm establishes in a new nest. In addition to exhib- iting greater locomotion, LQs respond to Figure 2. The vibration signal activity performed vibration signals with significant increases in on a laying queen during the swarm-preparation the rates of cell inspection and egg laying period. (Schneider, 1991). The signal may therefore facilitate laying activity during the period in Laying queens are vibrated only in the 3– which ovarian development must decline in 4 week interval when a colony is preparing to preparation for LQ flight. swarm. During this period, LQs are vibrated at Vibration signals can be performed on an increasing rate, and by the final 1–2 days queen cells and virgin queens throughout the before swarm departure they may receive rearing and elimination phases of the queen hundreds of signals each hour (Fig. 2) (Allen, replacement process. Workers often perform 1958, 1959a; Fletcher, 1975; Schneider, 1991; the signal on sealed queen cells, sometimes at Painter-Kurt and Schneider, 1998b). Fletcher very high rates. Several authors have reported (1975) suggested that vibration signals inhibit that queen cells are vibrated repeatedly when queen activity and are used by workers to VQs are attempting to emerge and that this prevent LQs from attacking developing queen may delay or prevent emergence (Bruinsma cells during the swarm-preparation period. et al., 1981; Fletcher, 1978a). VQs that are However, LQs can be vibrated for several days allowed to emerge sooner may have a before queen cells are present (Fig. 2), competitive advantage in eliminating rivals suggesting that preventing attacks is not the (Schneider et al., 2001; Schneider and sole function of the signal. Rather, most DeGrandi-Hoffman, 2002). Thus, workers evidence suggests that a primary role of the could potentially use the vibration signal to vibration signal during swarming preparations influence the timing of queen emergence and is to help gradually prepare laying queens for the ultimate outcome of the replacement proc- flight (Allen, 1958, 1959a; Schneider, 1991). ess. However, Grooters (1987) and Schneider LQs receive more vibration signals when and DeGrandi-Hoffman (2002) found no clear inactive than active and respond by walking or association between the signal and VQ emer- running (Schneider, 1991). Also, during gence order, while Schneider et al. (2001) swarm-preparation periods, workers decrease found an effect in some colonies but not oth- the rate at which LQs are fed (Allen, 1960; ers. Queen cells can be vibrated for 4–5 days Schneider, 1990). The combination of before emergence, suggesting that delaying increased activity and reduced food intake or preventing emergence is not the sole func- results in a noticeable weight loss that may be tion of the signal. Schneider and DeGrandi- necessary for laying queens to become Hoffman (2002) found that queen cells airborne (Allen, 1958; Schneider, 1991). vibrated at higher rates were more likely to In addition to increased locomotion, vibra- develop to emergence, whereas those receiv- tion signals may also influence other aspects ing few or no vibration signals had a greater of LQ behavior associated with swarming. likelihood of being destroyed by workers LQs never leave the nest normally and may before development was completed. The sig- pay little or no attention to stimuli associated nal may therefore help to promote develop- with the outside world. If vibration signals ment, although its specific effect on queen influence response thresholds, then they may cells is unknown. Indeed, the role of the signal make LQs more likely to react to stimuli that during queen rearing remains one of the least 124 S.S. Schneider, L.A. Lewis understood aspects of vibration activity in DeGrandi-Hoffman, 2003), relatedness cues honey bee colonies. (Tarpy and Fletcher, 1998), reproductive Vibration signals are also performed on capacities (Tarpy et al., 2000), or VQ size and VQs after they emerge. However, there is tre- fighting ability (Grooters, 1987; Hatch et al., mendous variability in the number of signals 1999; Bernasconi et al., 2000). However, we performed on different queens in the same col- have a limited understanding of the impor- ony. Some may be vibrated at rates of 200– tance of these factors in determining worker- 300 signals per hour, while others receive few queen interactions (Tarpy and Gilley, 2004). or no signals (Gilley, 2001; Schneider et al., Experimental manipulations of queen charac- 2001). VQs that are vibrated at higher rates teristics will be necessary to determine the fac- relative to their sister queens survive longer, tors that stimulate signal performance and to eliminate more rivals and are more likely to fully evaluate the relationship between vibra- become the new laying queens of their colo- tion activity and VQ success. nies (Schneider et al., 2001, 2002; Schneider Influencing aggressive interactions is prob- and DeGrandi-Hoffman, 2003). VQs receive ably not the only function of the signal during more signals when inactive and respond with queen competition. VQs can be vibrated at increased locomotion (Schneider, 1991; but high rates more or less continuously for days, see Fletcher, 1978a). In particular, VQs are and it seems unlikely that such continuous sig- often vibrated at high rates when near rivals, naling would be necessary to regulate only which elicits brief bursts of running that may occasional interactions. Furthermore, VQs remove them from potential battles and tem- continue to receive vibration signals after the porarily prevent fighting. VQs can also rival elimination period is completed. Signal- respond to the vibration signal by producing a ing activity often increases shortly before VQs pulsed sound called “piping” (Fletcher, 1978a; depart on mating flights (Fletcher, 1978a; Schneider, 1991; Gilley, 2001). While the Schneider, unpublished data) and continues function of piping is not well understood, it until egg laying begins. Vibration signals may may advertise fighting ability and inhibit the therefore allow workers to influence not only emergence of rivals (Visscher, 1993). Queens rival interactions, but also mating flight activ- confined in their cells are often killed by ity and the onset of oviposition by VQs. emerged VQs (Gilley, 2001; Schneider et al., Thus, as has been demonstrated for work- 2001; Schneider and DeGrandi-Hoffman, ers, the vibration signal may act as a nonspe- 2003). Thus, the stimulation of piping by cific modulator of queen behavior. By influ- the vibration signal could further promote the encing locomotor activity, development, fighting success of certain VQs and influence emergence, aggressive interactions, flight the outcome of the queen replacement process behavior and oviposition, the signal may allow (Schneider et al., 2001; Schneider and workers to coordinate numerous aspects of DeGrandi-Hoffman, 2003). The vibration sig- queen behavior with colony-level reproduc- nal may therefore give workers a degree of tive decisions. control over the behavior of VQs that helps to determine which queen will inherit the natal nest. 3.3. House hunting by honey bee However, the cause-and-effect relationship swarms between the vibration signal and VQ success is unclear. The signal might enhance the survival A final cooperative activity that is influ- of queens that are vibrated at higher rates, per- enced by the vibration signal is the process of haps by delaying their interactions until they house hunting, in which a swarm of honey have greater maturity and fighting ability. bees chooses and moves to a new nest cavity. Alternatively, the signal could be used to pro- House hunting consists of two main stages. tect less-vibrated VQs, by temporarily thwart- First, scout bees must locate a variety of poten- ing the attacks of opponents that are vibrated tial nest cavities and then winnow the choices more. The tendency of workers to vibrate down to a single selection. Next, after a cavity some queen more than others could potentially has been chosen, the entire swarm must lift off be influenced by paternity (Schneider and en masse and relocate to the selected site. Vibration signal and modulatory communication 125

The house-hunting process therefore involves cluster. Recipients respond with heightened a series of collective decisions and is control- locomotion and an increased tendency to fly, led by at least four different communication so that as liftoff approaches the entire swarm signals (see Seeley and Visscher, 2004). appears to be in motion and this activity culmi- Waggle dances are performed by scout bees on nates in mass flight (Lewis and Schneider, the surface of swarm clusters and communi- 2000). cate the location of potential nest cavities. Ini- Donahoe et al. (2003) experimentally con- tially a variety of sites are communicated, but firmed the role of the signal in swarm liftoff typically all waggle dance activity becomes and movement by removing vibrating bees focused on one location, which represents the throughout the house-hunting process. The new site to which the swarm will relocate removal of vibrators increased the duration of (Lindauer, 1955; Seeley and Buhrman, 1999; the lift-off preparation periods by 4–7 times, Camazine et al., 1999; Visscher, 2003). Once caused liftoff attempts to be aborted, and for large numbers of recruits are visiting one par- some swarms may have hindered the ability to ticular nest site, which usually coincides with move to the chosen nest site once they become the onset of consensus among waggle dancers, airborne. Vibrator removal did not affect the some scouts begin producing a pulsed sound ability of swarms to maintain the high levels of called “wings-together worker piping” (hence- consensus waggle dancing and piping that forth referred to as piping) on the swarm clus- normally precede departure. The observed ter (Seeley and Visscher, 2003). Piping is per- changes to liftoff behavior may therefore have formed at an increasing rate throughout the resulted directly from diminished vibration final hour or so in which the swarm is prepar- signal activity. ing for departure, and may cause recipients to Despite the altered liftoff and movement warm their thoracic muscles to a flight-ready behavior resulting from the removal of vibra- temperature (Seeley and Tautz, 2001). Addi- tors, all experimental swarms ultimately relo- tionally, shortly before departure some bees cated to a new nest site (Donahoe et al., 2003). begin to perform “buzz running”, which con- However, this occurred only after prolonged sists of a worker running over the swarm in a periods of consensus dancing and piping. zigzag pattern while buzzing its wings every These results suggest that the vibration signal second or so (Lindauer, 1955; Esch, 1967). may not be essential for the successful com- Buzz running may trigger the final break up of pletion of house hunting, but it is necessary for the cluster for liftoff (Lindauer, 1955; Martin, the process to happen quickly and efficiently. 1963), although its role in swarming is unclear By generating increased activity in all work- (Camazine et al., 1999). A fourth signal ers, the signal may enhance responsiveness to involved in house hunting is the vibration sig- waggle dances, piping and buzz running, and nal, which is performed from the time the clus- may thereby help to integrate the effects of the ter first forms until the moment of swarm suite of signals used to formulate decisions for departure (Schneider et al., 1998; Visscher et swarm liftoff and movement (Donahoe et al., al., 1999; Lewis and Schneider, 2000). House 2003). hunting therefore provides an excellent oppor- The vibration signal may also influence the tunity to explore how the vibration signal nest-site selection stage of house hunting. interacts with other communication signals to Most signals produced on swarms are per- formulate and adjust collective decisions in formed by bees of foraging age (Lewis and honey bees. Schneider, 2000) and this is also the age group Several recent studies suggest that the that contains the majority of nest-site scouts vibration signal plays a major role in swarm (Gilley, 1998). About 20% of vibrating bees liftoff and movement behavior (Visscher et al., perform waggle dances for nest sites, which 1999; Lewis and Schneider, 2000). Vibration suggests an immediate association of the sig- activity often increases dramatically during nal with scouting and recruitment (Visscher the final 30–60 min before departure. During et al., 1999; Lewis and Schneider, 2000). In the liftoff-preparation period, numerous work- addition, vibrated recipients have an increased ers perform long series of vibration signals probability of contacting nest-site dancers and while weaving repeatedly into and out of the flying from the swarm (Lewis and Schneider, 126 S.S. Schneider, L.A. Lewis

2000). Thus, during the first phase of house How might the proposed function of the hunting, a portion of vibrators are direct par- vibration signal be examined experimentally? ticipants in nest-site selection and their signals If the signal operates to enhance coordination could work in conjunction with waggle dances among activities, then vibration activity to recruit workers to potential nest sites. How- should increase in situations where greater ever, vibration signals are equally likely to be synchronization is required among different performed by waggle dancers for all sites, sug- worker groups. There are at least three events gesting that signaling activity is not used to that occur naturally in honey bee colonies in help focus recruitment on the one site that is which such increased behavioral integration ultimately selected for the new nest (Schneider may become necessary. First, when colonies et al., 1998). Similarly, the removal of vibrat- begin to emerge from overwintering, the ing bees does not alter the overall level of wag- resumption of brood rearing must be carefully gle dance activity observed, the time required balanced with the energy constraints that to achieve consensus for a nest site, or the rate arise from dwindling food reserves, dimin- at which new dancers for the chosen site are ished worker populations, and limited floral recruited (Donahoe et al., 2003). Thus, the role resources during late winter and early spring. of the vibration signal in nest-site selection is Such conditions may require a greater level of unclear. Future studies should focus on the coordination among worker groups than typi- effect that the vibration signal may have on the cally occurs in colonies that are buffered by number of potential nest sites visited, the area large food reserves and worker numbers. of the environment searched for suitable cavi- Indeed, vibration activity is often greater in ties, and the distribution of recruits among colonies in early spring compared to late sum- sites. mer (Schneider, personal observation). Simi- larly, greater synchronization among tasks may also be required when a swarm founds a 4. THE ROLE OF MODULATORY new nest. Initially, the energy reserves of the SIGNALS IN COOPERATIVE swarm consist almost entirely of the food that ACTIVITIES workers have stored in their crops, and brood rearing and food processing cannot begin until While the vibration signal influences food comb has been constructed. Furthermore, collection, foraging-related tasks, queen rapid colony establishment and growth are replacement, swarming and house hunting, essential to develop the large worker popula- many of these cooperative actions can occur tions and amass the huge food reserves needed with little or no vibration activity (Schneider for winter survival (Seeley and Visscher, et al., 1986a; Gilley, 2001; Schneider et al., 1985). Thus, during the initial phase of colony 1998, 2001). Why then is a non-specific signal founding it may be particularly important that sometimes used to help orchestrate coopera- energy budgets remain finely balanced, so that tive activities, when other specific signals and resources devoted to comb building do not cues exist that alone are sufficient to regulate compromise brood rearing, or that food collec- these behaviors? Perhaps the primary function tion does not outstrip comb construction and of the vibration signal is to make fine-tuned the ability to store and process harvested adjustments to colony-level decisions. By resources (see Pratt, 2004). Although the altering contact with and perhaps responsive- vibration signal activity of newly founded ness to other stimuli, the signal could help to nests has never been examined, it would be adjust the degree of behavioral integration expected to increase if this facilitates respon- within and among worker groups, and thus to siveness to other stimuli and promotes the more closely synchronize the interactions nec- integration of tasks that must be coordinated essary for cooperative efforts. Such a function with limited energy reserves. would be consistent with the general effects of A third situation that could necessitate the signal, its use in a variety of contexts, its increased behavioral integration may occur frequent interaction with other specific signals when afterswarms are produced during colony and cues, and its facilitating, but nonessential, reproduction. In colonies that produce after- role in colony activities. swarms, not only must one or more VQs Vibration signal and modulatory communication 127 depart with portions of the worker population, Partan and Marler, 1999; Donahoe et al., but VQ aggressive interactions must be con- 2003). Indeed, modulation may be necessary trolled to ensure that some queens remain alive in any system in which individual units that act for the continuation of the natal nest following on only local information must interact within swarm departure (Visscher, 1993). The rate at and among subgroups to generate global which queens receive vibration signals is typi- responses. For example, neuromodulation is a cally much greater in colonies that are produc- characteristic of all animal nervous systems. ing swarms and afterswarms than in those Neuromodulators do not generate specific replacing their queens in association with responses, but rather alter the excitability and supercedure or queen loss (Schneider et al., intrinsic properties of neurons and influence 2001). This greater vibration activity may help sensitivity to other inputs. These changes, in to synchronize more closely the behavior of turn, modify the strength, duration and nature different VQs with colony activities associated of subsequent activity (Katz, 1995, 1998; with the afterswarming process. Thus, over- Marder and Thirumalai, 2002). Neuromodula- wintering, colony establishment and after- tion can contribute to the fine-tuning of indi- swarming may provide valuable opportunities vidual neuronal circuits and to the organiza- to assess experimentally the role of modula- tion of ensembles of circuits scattered tory signals in collective decision making and throughout the nervous system, which can ulti- examine how different types of signals interact mately change an animal’s behavioral state to organize labor during different phases of the (Katz, 1999; Marder and Thirumalai, 2002). annual cycle of honey bee colonies. The responsiveness and flexibility of neural Modulatory communication may be an pathways cannot be fully understood without important factor in the regulation of many incorporating the effects of neuromodulation (Marder and Thirumalai, 2002). In a similar social interactions that involve multicompo- manner, we may not be able to fully appreciate nent systems of communication (Beshers the subtleties and adaptability of cooperative et al., 1999; Hölldobler, 1995, 1999; Partan activities in social animals unless we take into and Marler, 1999). For example, in numerous account the role of modulatory communica- species of highly social insects, cooperative tion in group decision making. The vibration activities such as foraging, brood care, nest signal therefore provides an excellent opportu- defense and colony movements are organized nity for increasing our knowledge, not only of by suites of chemical and tactile signals the complexity of honey bee communication, (Hölldobler and Wilson, 1990; Hölldobler but also of the mechanisms by which modula- et al., 1996; Roces and Hölldobler, 1996; tory effects are incorporated into the coopera- Savoyard et al., 1998). The tactile signals are tive activities of highly social animals in often “vibration like”, in that they involve general. rapid oscillatory movements of the signaler’s body and elicit increased activity in recipients by altering responsiveness to other stimuli Résumé – Signal de vibration, communication modulatrice et organisation du travail chez (reviewed in Schneider et al., 1986a; l’Abeille domestique, Apis mellifera. Les activités Hölldobler, 1995, 1999). These signals fre- de coopération chez les abeilles domestiques néces- quently function as “catalysts” (sensu Robson sitent la coordination de nombreux groupes and Traniello, 1999), in that their performance d’ouvrières accomplissant des tâches étroitement is not required for a cooperative activity to liées, mais qui répondent à divers stimuli, contrô- occur, but their presence increases the rate at lent divers aspects de l’environnement de la colonie et peuvent être répartis dans divers endroits du nid. which the group behavior proceeds. Thus, Un défi central de l’étude de la socialité des abeilles modulatory signals may often help to make domestiques est de comprendre les signaux de com- fine-tuned adjustments to cooperative activi- munication utilisés pour intégrer le comportement ties in social insects that are dependent upon au sein et entre les groupes d’ouvrières. Les collective responses to sets of communication « signaux de communication modulatrice » peuvent signals (Hölldobler, 1999). The modulation of être importants pour parvenir à l’intégration com- portementale, parce qu’ils influencent de nombreu- responsiveness to other stimuli may also be a ses ouvrières, suscitent un accroissement général de feature of many vertebrate species that operate l’activité et peuvent être utilisés dans une large collectively (McGurk and MacDonald, 1976; gamme de contextes. Les signaux modulateurs 128 S.S. Schneider, L.A. Lewis peuvent donc influencer simultanément de nom- entre sous-groupes pour produire des réactions breuses tâches et aider à coordonner l’activité parmi importantes. Le signal de vibration fournit donc un les ouvrières qui accomplissent des tâches interdé- excellent système pour étudier non seulement la pendantes. complexité du système de communication de Le « signal de vibration » de l’Abeille domestique l’Abeille domestique, mais aussi le rôle de la modu- est un exemple de signal de communication modu- lation dans les activités de coopération en général. latrice. Il est exécuté en réaction à une variété de sti- muli, il est dirigé vers les ouvrières de tous âges et Apis mellifera / signal de vibration / communica- suscite une augmentation générale de l’activité qui tion modulatrice / décision collective / signal s’exprime souvent par une locomotion accrue. Le multimodal signal provoque également un accroissement des tâches accomplies. Les plus vieilles ouvrières qui Zusammenfassung – Vibrationssignal, modulie- reçoivent les signaux de vibration ont une probabi- rende Kommunikation und Organisation der lité accrue de s’engager dans la récolte de nourriture Arbeit bei Honigbienen, Apis mellifera. Die aufei- et les plus jeunes à passer plus de temps aux travaux nander abgestimmten Aktivitäten der Honigbienen d’intérieur tels que les soins au couvain, le traite- benötigen eine Koordination von vielen Arbeits- ment du nectar et du pollen et la manipulation des gruppen, die voneinander abhängende Aufgaben rayons. Le signal peut influencer le comportement durchführen, die aber auf unterschiedliche Reize de l’ouvrière en modifiant sa sensibilité à d’autres reagieren, die unterschiedliche Aspekte der signaux et stimuli, qui en retour déclenchent des Umweltbedingungen des Volks wahrnehmen und actions données. Le message du signal semble être die vielleicht unterschiedlich im Nest verteilt sind. « augmentez votre activité », ce qui, combiné à Eine zentrale Herausforderung bei der Erforschung l’âge, au génotype et à la condition physiologique des Sozialstaats der Honigbienen ist das Verständ- de la réceptrice, conduit à des réactions spécifiques. nis der Kommunikationssignale für eine Abstim- Le signal de vibration est donc bien adapté pour mung des Verhaltens innerhalb und zwischen den influencer simultanément de nombreuses tâches et Arbeiterinnengruppen. „Signale für eine modulie- intégrer le comportement de groupes d’ouvrières rende Kommunikation“ sind wichtig, um diese Inte- qui accomplissent des tâches étroitement liées. gration im Verhalten zu erreichen, weil sie viele Le signal de vibration peut aider à ajuster au moins verschiedene Arbeiterinnen erreichen, einen gene- trois activités de coopération des colonies rellen Anstieg der Aktivität hervorrufen und in vie- d’abeilles. Une grande partie des signaux de vibra- len verschiedenen Zusammenhängen benutzt wer- tion est associée au butinage. Les structures journa- den können. Modulierende Signale können daher lières d’activité vibratoire peuvent aider à ajuster la viele Aufgaben gleichzeitig beeinflussen und könn- récolte de nourriture et les tâches liées au butinage ten so helfen, die Aktivitäten von Arbeiterinnen zu aux variations à court et à long terme de l’abon- koordinieren, die unterschiedliche Aufgaben haben. dance florale et des réserves énergétiques de la Ein Beispiel für modulierende Kommunikationssi- colonie (Fig. 1). Des signaux de vibration sont éga- gnale ist das „Vibrationssignal“ der Honigbienen. lement produits pour les reines lors de l’essaimage Es tritt als Reaktion auf eine Vielzahl von Reizen et de la supersédure. Les signaux peuvent aider à auf, betrifft Arbeiterinnen aller Altersstufen, und préparer les reines pondeuses à s’envoler (Fig. 2), à ruft einen allgemeinen Anstieg der Aktivität hervor, influencer le développement et l’émergence de der häufig eine vermehrte Bewegung hervorruft. reines vierges et agit sur l’issue de la rivalité entre Das Signal bewirkt auch eine verstärkte Arbeitsleis- reines vierges, pouvant ainsi aider à déterminer tung. Bei älteren Arbeiterinnen, die das Vibrations- quelle reine héritera du nid. Enfin des signaux de signal wahrnehmen, steigt die Wahrscheinlichkeit vibration sont également produits lorsqu’un essaim zu Sammelflügen. Jüngere verbringen mehr Zeit est à la recherche d’un nouveau nid. Le signal mit Aktivitäten im Innendienst, wie Brutpflege, est nécessaire pour qu’il s’envole rapidement et Futterverarbeitung und Bearbeitung der Waben. s’installe avec succès dans le nouveau site de Das Signal kann das Verhalten der Arbeiterinnen nidification. durch eine Änderung der Reaktion auf andere Le signal de vibration peut donc interagir avec Signale und Reize beeinflussen, wodurch wiederum d’autres signaux et stimuli pour aider à accorder bestimmte Aktionen hervorgerufen werden. Die avec précision les décisions collectives qui régulent Botschaft dieses Signals scheint zu sein: „steigere les activités de coopération des abeilles. Les deine Aktivität“, was in Kombination mit dem signaux qui fonctionnent comme le signal de vibra- Alter, dem Genotyp und den physiologischen tion sont largement répandus chez les insectes Bedingungen der Empfänger zu speziellen Reaktio- sociaux supérieurs, ce qui laisse penser que la com- nen führt. Deshalb ist das Vibrationssignal gut ge- munication modulatrice peut constituer une compo- eignet gleichzeitig eine Vielzahl von Arbeiten zu sante importante dans de nombreuses interactions beeinflussen und das Verhalten von Gruppen zu de coopération qui impliquent des systèmes de integrieren, die voneinander unabhängige Aufga- communication multicomposants. En fait la modu- ben durchführen. lation peut être nécessaire dans tout système où des Das Vibrationssignal könnte helfen, mindestens unités individuelles doivent interagir à l’intérieur et drei kooperative Aktivitäten der Bienenvölker Vibration signal and modulatory communication 129 aufeinander abzustimmen. Ein Großteil der Vibra- Beshers S.N., Robinson G.E., Mittenthal J.E. (1999) tionssignale beeinflusst das Sammelverhalten. Response thresholds and division of labor in Tägliche Muster von Vibrationsaktivität könnten insect colonies, in: Detrain C., Deneubourg J.L., helfen, Nahrungseintrag und trachtabhängige Pasteels J.M. (Eds.), Information processing in Aufgaben aufeinander abzustimmen und zwar bei social insects, Birkhäuser Verlag, Berlin, zwei Dingen, kurzzeitige oder andauernde Ände- pp. 115–139. rungen im Blütenangebot und in den Energiereser- Biesmeijer J.C. (2003) The occurrence and context of ven im Volk (Abb. 1). Vibrationssignale werden the shaking signal in honey bees (Apis mellifera) auch für Königinnen während des Schwärmens und exploiting natural food sources, 109, bei Umweiselung gegeben. Die Signale könnten 1009–1020. helfen, legende Königinnen auf den Flug vorzube- Bruinsma O., Kruijt J.P., van Dusseldorp W. (1981) reiten (Abb. 2), die Entwicklung und den Schlupf Delay of emergence of honey bee queens in von Jungköniginnen zu beeinflussen und Auswir- response to tooting sounds, Proc. Kon. Ned. kungen beim Ausgang im Wettkampf der Jungköni- Akad. Wet. C. 84, 381–387. ginnen zu haben und damit einen Einfluss darauf Camazine S., Visscher P.K., Finley J., Vetter R.S. zu haben, welche Königin das Nest übernimmt. (1999) House-hunting by honey bee swarms: Schließlich werden Vibrationssignale auch aus- collective decisions and individual behaviors, geübt, wenn ein Bienenschwarm eine Nisthöhle Insectes Soc. 46, 348–360. sucht. Das Signal ist für einen schnellen und erfolg- Camazine S., Deneubourg J.-L., Franks N.R., Sneyd reichen Start und den Einzug in das neue Nest J., Theraulaz G., Bonabeau E. (Eds.) (2001) Self- notwendig. Damit könnte das Vibrationssignal organization in biological systems, Princeton andere Signale und Reize beeinflussen, um eine Univ. Press, Princeton, NJ. feine Abstimmung bei kollektiven Entscheidungen Donahoe K., Lewis L.A., Schneider S.S. (2003). The bei der Regulation von sozialen Aktivitäten der role of the vibration signal in the house-hunting Honigbienen zu ermöglichen. Signale mit Funktio- process of honey bee (Apis mellifera) swarms, nen wie das Vibrationssignal sind in hoch sozialen Behav. Ecol. Sociobiol. 54, 593–600. Insekten weit verbreitet. Das deutet darauf hin, dass eine modulierende Kommunikation eine wichtige Elekonich M.M., Schulz D.J., Bloch G., Robinson Komponente in vielen kooperativen Interaktionen G.E. (2001) Juvenile hormone levels in honey bee (Apis mellifera L.) foragers: foraging experience sein könnte, die beim von vielen Komponenten and diurnal variation, J. Insect Physiol. 47, 1119– abhängigen Kommunikationssystem beteiligt sind. 1125. In der Tat, eine Notwendigkeit der Modulation scheint in jedem System zu bestehen, in dem ein- Esch H. (1967) The sounds produced by swarming zelne Einheiten innerhalb und zwischen Untergrup- honey bees, Z. Vergl. Physiol. 56, 408–411. pen interagieren, um wichtige Reaktionen zu veran- Fletcher D.J.C. (1975) Significance of dorsoventral lassen. Das Vibrationssignal stellt somit ein abdominal vibration among honey-bees (Apis ausgezeichnetes System dar, um nicht nur die Kom- mellifera L), Nature 256, 721–723. plexität des Kommunikationssystems, sondern auch Fletcher D.J.C. (1978a) The influence of vibratory die Bedeutung der Modulation bei allgemeinen dances by worker honeybees on the activity of kooperativen Aktivitäten zu untersuchen. virgin queens, J. Apic. Res. 17, 3–13. Fletcher D.J.C. (1978b) Vibration of queen cells by Vibrationssignal / modulierende Kommunika- worker honeybees and its relation to the issue of tion / kollektive Entscheidungen / Apis mellifera / swarms with virgin queens, J. Apic. Res. 17, multimodulierende Signale 14–26. Frisch K. von (1967) The dance language and orientation of bees, Harvard Univ. Press, REFERENCES Cambridge, Mass. Allen M.D. (1958) Shaking of honeybee queens prior Gahl R. (1975) The shaking dance of honeybee to flight, Nature 181, 68. workers: evidence for age discrimination, Anim. Behav. 23, 230–232. Allen M.D. (1959a) The occurrence and possible significance of the ‘shaking’ of honeybee queens Gilley D.C. (1998) The identity of nest-site scouts in by workers, Anim. Behav. 7, 66–69. honey bee swarms, Apidologie 29, 229–240. Allen M.D. (1959b) The ‘shaking’ of worker Gilley D.C. (2001) The behavior of honey bees (Apis honeybees by other workers, Anim. Behav. 7, mellifera ligustica) during queen duels, Ethology 233–240. 107, 601–622. Allen M. (1960) The honey bee queen and her Grooters H.J. (1987) Influences of queen piping and attendants, Anim. Behav. 8, 201–208. worker behaviour on the timing of emergence of Bernasconi G., Ratnieks F.L.W., Rand E. (2000) honey bee queens, Insectes Soc. 34, 181–193. Effect of “spraying” by fighting honey bee Hammann E. (1957) Wer hat die Initiative bei den queens (Apis mellifera) on the temporal structure Ausflügen der Jungkönigin, die Königin oder die of fights, Insectes Soc. 47, 21–26. Arbeitsbienen? Insectes Soc. 4, 91–106. 130 S.S. Schneider, L.A. Lewis

Hatch S., Tarpy D.R., Fletcher D.J.C. (1999) Worker Beitrag zum Problem der Wanderschwärme, regulation of emergency queen rearing in honey Insectes Soc. 10, 13–42. bee colonies and the resultant variation in queen McGurk H., MacDonald J. (1976) Hearing lips and quality, Insectes Soc. 46, 372–377. seeing voices, Nature 264, 746–748. Haydak M.H. (1929) Some new observations on the Milum V.G. (1955) Honey bee communication, Am. bee life, Ceský Vcel. 63, 133–135. Bee J. 95, 97–104. Haydak M.H. (1945) The language of the honeybees, Nieh J.C. (1998) The honey bee shaking signal: func- Am. Bee J. 85, 316–317. tion and design of a modulatory communication Hölldobler B. (1995) The chemistry of social signal, Behav. Ecol. Sociobiol. 42, 23–36. regulation: Multicomponent signals in Painter-Kurt S., Schneider S.S. (1998a) Age and societies, Proc. Natl. Acad. Sci. USA 92, 19–22. behavior of honey bees, Apis mellifera Hölldobler B. (1999) Multimodal signals in ant com- (Hymenoptera: Apidae), that perform vibration munication, J. Comp. Physiol. A 184, 129–141. signals on workers, Ethology 104, 457–473. Hölldobler B., Wilson E.O. (1990) The , Harvard Painter-Kurt S., Schneider S.S. (1998b) Age and University Press, Cambridge, Mass. behavior of honey bees, Apis mellifera Hölldobler B., Janssen E., Bestmann H.J., Leal I.R., (Hymenoptera: Apidae), that perform vibration Oliveira P.S., Kern F., König W.A. (1996) signals on queens and queen cells, Ethology 104, Communication in the migratory -hunting 475–485. ant Pachycondyla (= Termitopone) marginata Partan S., Marler P. (1999) Communication goes (Formicidae, Ponerinae), J. Comp. Physiol. A multimodal, Science 283, 1272–1273. 178, 47–53. Pratt S. (2004) Collective control of the timing and Huang Z.-Y., Robinson G.E. (1999) Social control of type of comb construction by honey bees (Apis division of labor in honey bee colonies, in: mellifera), Apidologie 35, 193–205. Detrain C., Deneubourg J.L., Pasteels J.M. (Eds.), Robson S.K., Traniello J.F.A. (1999) Key individuals Information processing in social Insects, and the organization of labor in ants, in: Detrain Birkhäuser Verlag, Berlin, pp. 165–186. C., Deneubourg J.L., Pasteels J.M. (Eds.), Katz P.S. (1995) Neuromodulation and motor pattern Information processing in social insects, generation in the crustacean stomatogastric Birkhäuser, Berlin, pp. 239–259. nervous system, in: Ferrell W.R., Proske U. Roces F., Hölldobler B. (1996) Use of stridulation in (Eds.), Neural control of movement, Plenum foraging leaf-cutting ants: mechanical support Press, New York, pp. 277–283. during cutting or short-range recruitment signal? Katz P.S. (1998) Neuromodulation intrinsic to the Behav. Ecol. Sociobiol. 39, 293–299. central pattern generator for escape swimming in Savoyard J.L., Gamboa G.J., Cummings D.L.D., Tritonia, Ann. New York Acad. Sci. 860, 181– Foster R.L. (1998) The communicative meaning 188. of body oscillations in the social , Polistes Katz P.S. (1999) What are we talking about? Modes fuscatus (Hymenoptera, Vespidae), Insectes Soc. of neuronal communication, in: Katz P.S. (Ed.), 45, 215–230. Beyond neurotransmission: neuromodulation and Schick W. (1953) Über die Wirkung von Giftstoffen its importance for information processing, auf die Tänze der Bienen, Z. Vergl. Physiol. 35, Oxford University Press, New York, pp. 1–28. 105–128. Lewis L.A., Schneider S.S. (2000) The modulation of Schneider S.S. (1985) The vibration dance of the worker behavior by the vibration signal during honey bee, Apis mellifera: communication house hunting in swarms of the honeybee, Apis associated with the regulation of foraging mellifera, Behav. Ecol. Sociobiol. 48, 154–164. activity, Ph.D. thesis, University of California, Lewis L.A., Schneider S.S., DeGrandi-Hoffman G. Davis. (2002) Factors influencing the selection of Schneider S.S. (1986) The vibration dance activity of recipients by workers performing vibration successful foragers of the honey bee, Apis signals in colonies of the honeybee, Apis mellifera (Hymenoptera: Apidae), J. Kans. mellifera, Anim. Behav. 63, 361–367. Entomol. Soc. 59, 699–705. Lindauer M. (1955) Schwarmbienen auf Wohnungs- Schneider S.S. (1987) The modulation of worker suche, Z. Vergl. Physiol. 37, 263–324. activity by the vibration dance of the honey bee, Marder E., Thirumalai V. (2002) Cellular, synaptic Apis mellifera, Ethology 74, 211–218. and network effects of neuromodulation, Neural Schneider S.S. (1989) Dance behaviour of successful Networks 15, 479–493. foragers of the African honeybee, Apis mellifera Markl H. (1985) Manipulation, modulation, informa- scutellata (Hymenoptera: Apidae), J. Apic. Res. tion, cognition: some of the riddles of communi- 28, 150–154. cation, in: Hölldobler B., Lindauer M. (Eds.), Schneider S.S. (1990) Queen behavior and worker- Experimental and sociobiol- queen interactions in absconding and swarming ogy, Fischer, Stuttgart, pp. 163–194. colonies of the African honey bee, Apis mellifera Martin P. (1963) Die Steuerung der Volksteilung scutellata (Hymenoptera: Apidae), J. Kans. beim Schwärmen der Bienen. Zugleich ein Entomol. Soc. 63, 179–186. Vibration signal and modulatory communication 131

Schneider S.S. (1991) Modulation of queen activity Seeley T.D., Buhrman S.C. (1999) Group decision by the vibration dance in swarming colonies of making in swarms of honey bees, Behav. Ecol. the African honey bee, Apis mellifera scutellata Sociobiol. 45, 19–31. (Hymenoptera: Apidae), J. Kans. Entomol. Soc. Seeley T.D., Tautz J. (2001) Worker piping in honey 64, 269–278. bee swarms and its role in preparing for liftoff, J. Schneider S.S., DeGrandi-Hoffman G. (2002) The Comp. Physiol. A 187, 667–676. influence of worker behavior and paternity on the Seeley T.D., Visscher P.K. (1985) Survival of development and emergence of honey bee honeybees in cold climates: the critical timing of queens, Insectes Soc. 49, 306–314. colony growth and reproduction, Ecol. Entomol. Schneider S.S., DeGrandi-Hoffman G. (2003) The 10, 81–88. influence of paternity on virgin queen success in Seeley T.D., Visscher P.K. (2003) Choosing a home: hybrid colonies of European and African how the scouts in a honey bee swarm perceive the honeybees, Anim. Behav. 65, 883–892. completion of their group decision making, Schneider S.S., Lewis L.A. (2003) Honey bee Behav. Ecol. Sociobiol. 54, 511–520. communication: the “tremble dance”, the Seeley T.D., Visscher P.K. (2004) Group decision “vibration signal” and the “migration dance”, in: making in nest-site selection by honey bees, Webster T. (Ed.), Monographs in honey bee Apidologie 35, 101–116. biology, Northern Bee Books, West Yorks, Great Seeley T.D., Weidenmüller A., Kühnholz S. (1998) Britain, Vol. 1, pp. 1–26. The shaking signal of the honey bee informs Schneider S.S., McNally L.C. (1991) The vibration workers to prepare for greater activity, Ethology dance behavior of queenless workers of the honey 104, 10–26. bee, Apis mellifera (Hymenoptera: Apidae), J. Tarpy D.R., Fletcher D.J.C. (1998) Effects of Insect Behav. 4, 319–322. relatedness on queen competition within honey Schneider S.S., Painter-Kurt S., DeGrandi-Hoffman bee colonies, Anim. Behav. 55, 537–543. G. (2001) The role of the vibration signal during Tarpy D.R., Gilley D.C. (2004) Group decision queen competition in colonies of the honeybee, making during queen production in colonies of Apis mellifera, Anim. Behav. 61, 1173–1180. highly eusocial bees, Apidologie 35, 207–216. Schneider S.S., Painter-Kurt S., DeGrandi-Hoffman Tarpy D.R., Hatch S., Fletcher D.J.C. (2000) The G. (2002) Regulation of virgin queen behavior by influence of queen age and quality during queen the vibration signal of the honey bee and its replacement in honeybee colonies, Anim. Behav. possible role in the Africanization process, in: 59, 97–101. Erickson E.H. Jr., Page R.E. Jr., Hanna A.A. Tarpy D.R., Gilley D.C., Seeley T.D. (2004) Levels of (Eds.), Proc. 2nd Int. Conf. on Africanized Honey selection in a social insect: a review of conflict Bees and Bee Mites, A.I. Root, Medina, Ohio, and cooperation during honey bee (Apis pp. 34–44. mellifera) queen replacement, Behav. Ecol. Schneider S.S., Stamps J.A., Gary N.E. (1986a) Sociobiol., in press, DOI 10.1007/s00265-003- The vibration dance of the honey bee. I. 0738-5. Communication regulating foraging on two time Visscher P.K. (1993) A theoretical analysis of scales, Anim. Behav. 34, 319–322. individual interests and intracolony conflict Schneider S.S., Stamps J.A., Gary N.E. (1986b) The during swarming of honey bee colonies, J. Theor. vibration dance of the honey bee. II. The effects Biol. 165, 191–212. of foraging success on daily patterns of vibration Visscher P.K. (2003) How self-organization evolves, activity, Anim. Behav. 34, 386–391. Nature 421, 799–800. Schneider S.S., Visscher P.K., Camazine S. (1998) Visscher P.K., Shepardson J., McCart L., Camazine Vibration signal behavior of waggle-dancers in S. (1999) Vibration signal modulates the behavior swarms of the honey bee, Apis mellifera of house-hunting honey bees (Apis mellifera), (Hymenoptera: Apidae), Ethology 104, 963–972. Ethology 105, 759–769. Seeley T.D. (1995) The wisdom of the hive, Harvard Winston M.L. (1987) The biology of the honey bee, University Press, Cambridge, Mass. Harvard University Press, Cambridge, Mass.