Insect. Soc. DOI 10.

1007/s00040-012-0224-z

Insectes Sociaux

REVIEW ARTICLE

The dance legacy of Karl von Frisch

M. J. Couvillon

Received: 2 August 2011 / Revised: 20 January 2012 / Accepted: 24 January 2012 International Union for the Study of Social Insects (IUSSI) 2012

nze der Abstract Karl von Frisch published Die Ta Bienen in 1946, which demonstrated that successful honey bee foragers perform a stereotyped dance to communicate the location of valuable resources to her nestmates. This discovery proved to be the starting point of many areas of investigation. Here I review some recent advancement in our understanding of the waggle dance. Keywords Waggle dance Honey bee foraging Recruitment Karl von Frisch Apis mellifera

Introduction In 1973, Karl von Frisch was awarded a Nobel Prize in Physiology for his discovery that honey bees communicate foraging locations to nestmates via the waggle dance (von Frisch, 1946). Although he was not the rst to ponder the bee recruitment phenomenon [Aristotle noticed each bee on her return (to a ower) is followed by three or four companions (Aristotle 350 B.C.)], von Frischs particular contribution decoded an invertebrates behavior into a symbolic language. These landmark experiments were controversial (Johnson, 1967; Wenner, 1967; Wenner et al., 1969; Gould, 1975; Munz, 2005) and groundbreaking. In the waggle dance, a returned forager bee advances linearly on the comb as she quickly vibrates her abdomen

M. J. Couvillon (&) The Laboratory of Apiculture and Social Insects (LASI), School of Life Sciences, The University of Sussex, Falmer, Brighton BN1 9QG, UK e-mail: M.Couvillon@Sussex.ac.uk

from side to side. This waggle run may last from \1 to 11 s, at which point she circles back (return phase) by turning alternating from the left or right until she is approximately at the start of her dance (Fig. 1). This circuit may be repeated a variable number of times (1 to [100) in a single dance bout, depending on resource quality (Seeley et al., 2000) (see below in Fine-tuning of the dance), and with each iteration, she communicates approximately the same distance and a direction from the nest site to a useful resource (nectar, pollen, water, propolis, or a new nest site) (von Frisch, 1946, 1967; Dyer, 2002). Distance and direction are encoded in the waggle run duration and orientation relative to vertical, respectively (von Frisch, 1946, 1967). Variation in angle and duration exists within these runs (Dyer, 2002; De Marco et al., 2008; Couvillon et al., submitted). Dance followers (recruits) take an average to derive a single distance and direction (von Frisch and Jander, 1957; Tanner and Visscher, 2008). That this dance could direct foragers to resources was astounding to scientists and non-scientists of that day. Language (or Language, as von Frisch diplomatically insisted in his writing) was considered under the exclusive jurisdiction of humans (Munz, 2005). Yet here were data demonstrating that not just an animal but an insect could inform her nestmates of a resources location. In the years since this seminal discovery, the waggle dance has been investigated in many different ways and has been used in many different applications, spurring a eld of research spanning basic science neurobiology to applied foraging ecology. Here I will review a few of the topics and developments that have occurred since von Frisch rst noticed that a single scout bee on a feeder quickly becomes an entire foraging group (von Frisch, 1923a,b, 1974).

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Fig. 2 In the round dance, a bee makes rapid circular movements, and each begins with a brief waggling of the abdomen (left side panel). The dancer will suddenly stop mid-circle and reverse her direction, only to circle in the opposite direction before reversing, and so on. Although the round dance may appear different from the waggle dance (right side panel) in that it lacks the linear stretch with the conspicuous body wagging, it actually is an extremely short version. Reprinted with permission (Gardner et al., 2008)

Fig. 1 A honey bee performs a waggle dance for four dance followers. Here the dancer performs a waggle run (1) followed by a turn to one side (2) to circle back (return phase) to the starting point of the waggle run (3). Then she begins another waggle run (4) and turns to the other side (5). This gure-of-eight circuit of waggle run ? return phase may be repeated [100 times. Illustration by N. Stadelmann, and reprinted ter and Farina, 2009a) with permission (Gru

Round dances and other recruitment signals In his writings, von Frisch described two types of dances: round and waggle dances. When a bee performs the former, she moves quickly in a circle, frequently reversing to move in the other direction (Fig. 2). In the latter, the gure-eight is further differentiated by a conspicuous waggle portion before the bee turns to the left or right (Tautz et al., 1996). Originally von Frisch believed the round dance communicated a nectar resource, whereas the waggle dance communicated a pollen resource (von Frisch, 1923b; Munz, 2005). This misunderstanding of the two types of dances arose from von Frischs training of bees to nectar feeders located near the hive, whereas pollen foragers exploited natural resources typically located at a greater distance from the hive. Later he would conclude that round dances were nondirectional recruitment for nearby resource, whereas the waggle dance gave directional information for resources located at distances more than 100 m (von Frisch, 1946, 1967). This notion of there being two categorically different types of dances persisted for decades. von Frisch himself noted that incremental increases in feeder distance resulted in the gradual transition from round to waggle (von Frisch, 1967; Gardner et al., 2008). Investigations into the acoustic component of dances provided excellent indirect evidence that the two dances were

actually a continuum of the same, encoded signal: dancers emit a train of short sound pulses that corresponds in length to the food source distance (Kirchner et al., 1988). Additionally, round dances contain a directional component, signicant even at 1 m (Kirchner et al., 1988). Jensen et al. likewise found a waggle component in round dances, signicant at 15 m (Jensen et al., 1997). However, nal evidence came from elegant analysis demonstrating rstly the presence of distance and direction in both round and waggle dances and secondly that there is a continuum between the two (Gardner et al., 2008). Authors conclude that honey bees have just one adjustable recruitment signal: the waggle dance (Gardner et al., 2008). Even as the round dance faced retirement, other signals were hired to the story. For example, as yin to the recruitment yang, we now know that honey bee recruitment, a positive feedback enhancement, also contains a brief, vibrational stop signal (Nieh, 1993; Lau and Nieh, 2009; Nieh, 2010). This signal, sometimes accompanied by a behavioral accoutrement akin to head butting, redirects foragers away from potentially dangerous sites (Nieh, 2010). Such a negative feedback has been shown both theoretically (Johnson and Nieh, 2010) and experimentally in bees and in other systems (Robinson et al., 2005; Nieh, 2010) to increase recruitment efciency by redirecting a workforce from harmful or nonprotable sites. Other components of the entire recruitment system are less understood. For example, a worker bee may grab the legs of other bees and vibrate her own body for a few seconds. The purpose of this shaking signal or even the context under which it occurs is currently unclear (Seeley et al., 1998; Biesmeijer, 2003a), even though the behavior has been extensively investigated (Allen, 1959; von Frisch, 1967; Schneider, 1986; Nieh, 1998; Seeley et al., 1998; Lewis et al., 2002). It is thought to function as a modulatory

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lldobler and Wilson, 1990; communication signal (Ho Biesmeijer, 2003a) to inuence the arousal of nestmate bees. For example, a successful forager, upon return to the hive, may shake her nestmates to spur her into greater activity (Allen, 1959; Schneider, 1986; Nieh, 1998; Seeley et al., 1998). However, shaking is also performed by unsuccessful foragers (Biesmeijer, 2003a). Therefore, it seems that the purpose of shaking and its intended meaning is subject to context and may be a broad cue for nestmates to reassess current activity (Biesmeijer, 2003a). Similarly, the tremble dance was previously thought to be a successful foragers response, upon her return to the hive, to a long delay for unloading her nectar (Seeley, 1992; Kirchner, 1993; Kirchner and Lindauer, 1994). However, tremble dances have also been observed by foragers returning from deteriorated or bad food sources (Lindauer, 1948). As such, similar to the shaking signal, there does not appear to be a single context under which the tremble dance occurs (Biesmeijer, 2003b).

Dance controversy and the role of odor and memory Flowers are fragrant and colorful. These adaptations exist to attract pollinators, and visitors like honey bees have evolved exquisite mechanisms by which to sense and to recall these oral features. Karl von Frisch was of course aware that the color and the odor of owers would be important for bees: his initial observations about honey bee recruitment occurred while he was demonstrating that bees, contrary to the thought of the day, possess color vision (von Frisch, 1914-1915, 1974). In 1967, odor played a major role in the doubts that Adrian Wenner and his student Dennis Johnson had about the waggle dance (Gould, 1975; Munz, 2005). Wenner and Johnson believed that odor, not a recruitment dance, was sufcient for foragers possessing an olfactory landscape to nd particular owers (Johnson, 1967; Wenner, 1967; Wenner et al., 1969). The resultant dialogue between Adrian Wenner and Karl von Frisch, reviewed by James Gould (Gould, 1975), was acrimonious at times (Munz, 2005). However, the dispute was largely resolved by the mid-70s, and most scientists now are convinced of the dance language (Seeley, 1991; Dyer and Smith, 1994; Srinivasan et al., 2000; Esch et al., 2001; Sherman and Visscher, 2002). The criticism, however, was important in spurring new research from both von Frisch and others to investigate the role of oral odors. For example, experiments using mechanical robot bees were only able to recruit successfully when scent was used both for the food in the feeder and in the samples given by trophallaxis to dance followers (Michelsen et al., 1989; Michelsen et al., 1992). Additionally, for a bee trained to a feeder containing scented food, the scent is

later sufcient to induce the same bee to return to that feeder. Scent therefore reactivates navigational memories (Reinhard et al., 2004). The importance of odor is also seen when an experienced forager encounters a conict between her own memory and a newly communicated (via the dance) unknown location. For example, scent comes off a dancers body while she is waggling; the scent may reactivate a dance followers previous memory (Reinhard et al., 2004) of a foraging location ter et al., 2008). In the face of that is not the danced one (Gru this information conict between a private, reactivated navigational memory and a social, communicated location, 93% of bees will opt to return to their remembered location ter et al., 2008). over the newly communicated one (Gru Why then do these foragers frequently follow many iterations of a dance before ultimately ignoring the message? And why do bees continue to dance if the information is not used? Clearly the information is useful, but the relative importance of the information may change in different contexts and environments. When dance information is experimentally obscured, colonies in temperate habitats do not experience a signicant decrease in foraging efciency; in contrast, colonies in a tropical forest are substantially impaired following this manipulation (Dornhaus and Chittka, 2004). Impressively, individuals themselves also adjust how (or how not) they use waggle dance information based on more immediate, short-term uctuations in resource availability. When a known food source becomes unrewarding, foragers then follow more waggle dances in the nest and successfully switch to ter and Ratnieks, 2011). Howthe danced food location (Gru ever, this switch is reluctant, demonstrating a remarkably con ter servative attitude in honey bees against exploration (Gru and Ratnieks, 2011). Overall, these data are important in explaining the apparent inefciency in dance recruitment ter and Farina, 2009a,b), which was (Riley et al., 2005; Gru one of the criticisms originally levied against the language (Johnson, 1967; Wenner, 1967). Ultimately the relative role of both odors and memory depends on the ecology and on the local availability of resources, which imparts a exibility well suited for efcient exploitation of ephemeral resources ter and Farina, (Gould, 1975; Dornhaus and Chittka, 1999; Gru 2009a). While the dance communication may sometimes be rendered unnecessary or inefcient against experience, it remains important for novice foragers. Sixty percent of ve foragers used waggle dance information to nd a food na source (Biesmeijer and Seeley, 2005). As the bee gains her own experiences, though, she uses the dance less, or she uses the dance to reactivate or to conrm her own foraging location memories (Biesmeijer and Seeley, 2005). However, even for experienced foragers, dance recruitment remains a useful way to guide a bee to a richer resource than

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she may herself discover (Seeley, 1983; Seeley and Visscher, 1988).

How do bees judge distance? One of the unknowns for von Frisch was how the forager judges the distance she has own. Karl von Frisch hypothesized that a bee monitored energy consumption during ight and converted this quantity into distance (von Frisch, 1967). However, adding weight to a honey bee does not cause her to over-estimate her distance, an inconsistency that led to the optic ow hypothesis (Esch and Burns, 1996). This hypothesis was strongly supported by an elegant experiment demonstrating that bees indeed measure distance by the amount of information that passes the retina during ight (Srinivasan et al., 2000). Bees were trained to y through tunnels with black stripes running parallel to the direction of ight, producing a landscape that is unchanging for the bee. These bees will experience less optical detail and perform, upon returning to the hive, dances indicating much shorter distances than expected. Likewise, bees were trained to y through tunnels with patterned stripes. These bees experience a landscape with a great amount of optical detail, and they will, upon returning to the hive, produce dances indicating much further distances than expected. The tunnels were identical in length. Any odometer is subject to noise. For example, bees ying over water, which gives less mean visual contrast compared to land, underestimate distance (Tautz et al., 2004). This is not surprising because, although bees have excellent trichromatic color vision (von Frisch, 1914-1915; Chittka et al., 2001), only the green receptor signal is used to estimate travel distance (Chittka and Tautz, 2003). Overall, the odometric signal is remarkably robust to most contrasts in the spatial landscape, an advantage for an animal frequently foraging over variable environments (Si et al., 2003). Finally, it was shown that the optic ow that informs foragers of distance does not inform for protability. These assessments of distance and protably (see below) are made and then they are communicated separately as different elements within the dance (Seeley et al., 2000; Shar and Barron, 2010).

Fine-tuning of the dance Within the dance itself, bees exercise incredible control over many details that then convey additional information to nestmates. For example, a dancer may adjust two different aspects of the dance to communicate resource quality

(Seeley et al., 2000). Firstly, resource protability is communicated by the number of intra-dance circuit (waggle phase ? return phase) iterations: higher quality resources translate into more circuits (Seeley, 1986; Seeley et al., 1991; Seeley, 1994; Seeley et al., 2000). Of course, in such a recruitment system, this results in longer-lasting dances, which affords more nestmates the opportunity to contact the dancer. Ultimately this results in more and more recruits being directed to a good resource (Seeley and Towne, 1992). Secondly, resource protability is communicated by the liveliness of the dance, specically the quickness of the return phase: higher quality resources translate into quicker return phases (Seeley et al., 2000). This nal point is important for ecologists who decode dances to determine foraging locations. If the quickness of the return phase is a function of resource quality, including the return phase in the actual dance duration when determining distance, as von Frisch did, makes the data noisy. Therefore, future studies that decode dances should focus on the information-rich waggle phase (Michelsen et al., 1992; Couvillon et al., submitted). Some of the best contributions to our understanding of how bees tune their foraging behavior were performed by von Frischs student Martin Lindauer, who made lasting advances to behavioral physiology and to our knowledge of the exibility and feedback loops of honey bee foraging (Seeley et al., 2002). It was already known that higher resource quality increases the probability of individual dancing (von Frisch, 1967); however, Lindauer demonstrated that individual threshold for dancing is adjusted in relation to food availability and, therefore, colony requirements (Lindauer, 1948; Seeley et al., 2002). At another time when a heating lamp was placed too close to an observation hive, Lindauer noticed that individual bees used evaporative cooling to lower temperatures and that the colony, depending on thermoregulatory needs, successfully balanced water supply with water demand. Upon further investigation, he determined that the queuing delays experienced when a returning forager wants to unload her crop of, for example, water to a receiving nestmate regulates her probability of dancing and, in turn, her likelihood of recruiting others to the resource (Lindauer, 1954; Seeley, 1994; Seeley and Tovey, 1994). This initial nding served as a starting point for many other investigations into queuing delays and their function in regulating foraging recruitment (Seeley and Tovey, 1994; Anderson and Ratnieks, 1999). Another lasting contribution of Lindauer came from his investigations into honey bee swarm nest site selection (Lindauer, 1955). As before, the discovery arose from a side observation: Lindauer noticed that bees dancing on a swarm carried neither pollen nor unloaded nectar. Additionally, the

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dancers were sooty and smelled like chimney sweeps (Seeley et al., 2002), which led Lindauer to suspect that the bees had been exploring cavities for a new nest site. To test this idea, Lindauer persuaded von Frisch to leave a swarm uncollected so he could observe the dances. From these observations, he saw the remarkable process of democratic deliberations for a new home (Seeley and Buhrman, 1999, 2001; Seeley, 2010). Although multiple scouts begin by initially advertising via dances many potential sites, over the next day, these multiple locations converge. Once consensus is reached, the swarm takes off in that direction (Lindauer, 1951, 1953, 1955). These data demonstrated beautiful evidence that animal groups may be an adaptive unit (Seeley et al., 2002; Seeley, 2010) capable of reaching an accurate, speedy, and unied decision (Seeley and Visscher, 2004).

Dance imprecision and the tuned-error hypothesis Variation exists between successive waggle runs of the same dance (Dyer, 2002; De Marco et al., 2008) Given that honey bees have had quite a long time to evolve this language (Dyer and Seeley, 1989; Dornhaus and Chittka, 1999) and considering that the language functions to direct nestmates to protable resources, why has evolution not selected against these errors? The tuned-error hypothesis suggested that the directional imprecision may be adaptiveand thus selected for because it tunes the dance to the spatial distribution of resources (Haldane and Spurway, 1954; Weidenmuller and Seeley, 1999). For example, a 4 angular scatter is sufcient to distribute recruits over a ower patch located nearby, whereas less angular scatter is sufcient to distribute recruits over a ower patch located further from the hive. Consistent with this hypothesis, it was shown that the recruits themselves spread a constant amount for 1001,000 m (Towne and Gould, 1988). Implicit in this assumption is the idea that oral resources typically occur in relatively large patches that may benet from a fanning of recruits; in contrast, new nest sites are at xed points. Dances for nest sites should therefore be more precise than dances for food. Indeed, it was shown that dance precision is higher for new nest sites compared to equidistant dances for food (Weidenmuller and Seeley, 1999; Dyer, 2002), providing support for an adaptive tuned-error hypothesis. However, dancers in the above scenarios were waggling on different substrates. When the same experiment was repeated on identical substrates, this difference in precision disappears (Tanner and Visscher, 2006). Additionally, nearby (\30 m) nest sites, which under the tuned-error hypothesis should be communicated precisely, contain either absent or limited directional information (Beekman et al., 2005). As

dances with visual reference are more precise, irrespective of distance (Tanner and Visscher, 2010), it seems more likely that dance scatter is an artefact of physical and performance constraints (Beekman et al., 2005; Tanner and Visscher, 2010). Dances for shorter distances means the duration of the waggle run may be \1 s. This necessitates the turning of the dancing bees body very quickly at the end of the waggle run to the left or right to circle back to her start point (Fig. 1), and this quick waggle run results in more angular divergence. Imprecision is therefore the simple consequence of the bee performing to the best of her ability. It may also be that undershooting each successive turn within a dance is more efcient for the dancer (Tanner and Visscher, 2008). Such a behavior would result in the described bi-modal clustering of angular scatter about the proper ight direction (Gardner et al., 2007; Tanner and Visscher, 2010). Lastly, the sun position itself may sometimes affect precision: in some parts of the world (e.g., near to the equator), the sun is directly overhead at solar noon, making directional information with respect to the solar azimuth difcult. Even as imprecision seems inevitable, bees display certain interesting compensatory features that appear to combat the problem. For example, it was noted that dancing either ceases or is disoriented just before and just after solar noon (Lindauer, 1961), a characteristic that von Frisch described as noontime laziness (von Frisch, 1967). However, it was later demonstrated that directional inaccuracy is highest when the sun is at its zenith (Gardner, 2007). Therefore, the described foraging hiatus may be an adaptive mechanism to reduce imprecision. Recruits may also play a role in reducing imprecision. Followers of the dance may be located either behind or alongside a dancer (Tanner and Visscher, 2009) and are known to follow a variable number of waggle runs. However, the number of followed waggle runs positively correlates with increased foraging ight accuracy (Tanner and Visscher, 2009). Additionally, it appears that dance followers average, which is a common method by which noise is reduced, the information from successive waggle runs (Tanner and Visscher, 2008), resulting in a vector that is as precise to the goal as if there were no divergence angle.

Other bees, Asian honey bees and the evolution of the dance The corbiculate bees are comprised of four tribes: Apini (honey bees, of which Apis is the only extant genus), Euglossini (orchid bees), Bombini (bumble bees) and Meliponini (stingless bees) (Thompson and Oldroyd, 2004). Both bumble bees and stingless bees possess forms of recruitment (Dornhaus and Chittka, 2001; Nieh, 2004). For example, although bumble bees do not communicate a resource

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location, they do successfully inform nestmates about a newly available food resource and its scent (Dornhaus and Chittka, 1999; Dornhaus and Chittka, 2001). A returning forager quickly zigzags across the nest (excited runs), a behavior that was shown to increase the likelihood that nestmates will themselves leave to forage (Dornhaus and Chittka, 2001). This behavior was shown to distribute a pheromone (Dornhaus et al., 2003; Granero et al., 2005). Although honey bees also use pheromones (Free, 1987), to date it has only been observed in other contexts and has not yet been shown to attract nestmates to a dance site. This difference suggests distinct evolutionary origins for bumble bee and honey bee resource recruitment (Granero et al., 2005). Meanwhile, the story in stingless bees is more complicated, mostly as the group consists of hundreds or even thousands of species in 36 genera (Michener, 2000). These species vary in many factors like colony size (from few dozen to many hundreds of thousands), nesting habitat (Sakagami, 1982; Roubik, 2006), and the resources that must be collected (e.g., pollen, nectar, resin, dead animals, mud) (Roubik, 1989; Nieh, 2004). Correspondingly, their recruitment systems range from excitatory non-directional recruitment to directional recruitment, including the communication of height (Lindauer and Kerr, 1958; Nieh, 2004), which honey bees do not do (Dyer, 2002). It is unknown whether the stingless bees are more closely related to the bumble bees, a hypothesis supported by molecular data (Sheppard and McPheron, 1991; Cameron, 1993; Koulianos et al., 1999; Cameron and Mardulyn, 2001), or if the stingless bees are more closely related to the honey bees, a hypothesis supported by morphological, behavioral, and biogeographical data (reviewed in Oldroyd and Wongsiri, 2006). These two alternative phylogenies (simultaneously incompatible, but consistent with respective data Oldroyd and Wongsiri, 2006) require resolution, especially if one is interested in recruitment. Without an understanding of the relationships within the corbiculate bees, the waggle dances evolutionary context is uncertain. As there is no immediate answer, let us therefore set aside this issue and focus just within Apini. Discussion to this point has been conned to Apis mellifera; however, the western honey bee is just one of nine species within Apis (Michener, 2000). The other eight extant species, known collectively as the Asian honey bees, provide excellent opportunities for comparative studies. Molecular, behavioral, morphological data have recently converged (Engel and Schultz, 1997; Arias and Sheppard, 2005; Oldroyd and Wongsiri, 2006; Rafudin and Crozier, 2007; Duangphakdee et al., 2011) to produce a probable phylogeny. In the consensus, the dwarf honey bees (Apis orea and A. andreniformis) represent the most basal state, whereas the Asian cavity nesters (Apis cerana, A. nigrocincta, and A. nuluensis) are the most derived. The giant Asian honey bees (Apis dorsata and A. laboriosa) represent

intermediate states (Oldroyd and Wongsiri, 2006; Rafudin and Crozier, 2007; Beekman et al., 2008). Additionally, this organization from basal to derived maps nicely with their corresponding increase in dance language complexity, an insight anticipated by Lindauer (Lindauer, 1956c,a; Dyer, 2002). Directional recruitment is particularly important for the Asian species as oral resources are distributed in patches throughout the tropical forest landscape (Dornhaus and Chittka, 1999; Dornhaus and Chittka, 2004; Oldroyd and Wongsiri, 2006). It seems likely that an ancestral species within Apis rst communicated a successful forage with something akin to the bumble bees excited runs (Dornhaus and Chittka, 2001). This recruitment may have included shaking its body before lift-off while aligning toward the protable forage (Dyer, 2002; Oldroyd and Wongsiri, 2006). In this way, the early waggle dance was a symbolic representation of the foraging ight (von Frisch, 1967; Wilson, 1971). Over time, this behavior became more stereotyped (Duangphakdee et al., 2011) and is thought ultimately to resemble the dance of the dwarf honey bees. These bees (Apis orea and A. andreniformis) are opennesters whose hive consists of a single, exposed comb under a tree limb or rock ledge (Michener, 2000). A portion of the comb wraps around the top of the limb to create a horizontal surface (Duangphakdee et al., 2011). Successful foragers dance on the at portion (Lindauer, 1956b,a) and, instead of referencing gravity, the dwarf honey bees point directly to their goal (Koeniger et al., 1982; Dyer, 1985a; Duangphakdee et al., 2011). As Apis diverged, the language added complexity in the form of two adaptations from the simple dance of the dwarf honey bees. The giant honey bees (Apis dorsata and A. laboriosa) are also open-nesters whose comb hangs from limbs or cliffs. However, their combs provide no horizontal surface, and dancers are thus unable to point directly at the goal. They evolved a solution: giant bee dancers, like their honey bee relatives, use gravity as a reference to the sun (Lindauer, 1956b; Morse and Laigo, 1969; Dyer and Seeley, 1991). Additionally, A. dorsata forage and dance nocturnally (Dyer, 1985b) or under a curtain of their own nestmates (Oldroyd and Wongsiri, 2006). This reduced visibility is compensated by an adaptive enhancement of the sound pulse during the waggle run (Kirchner and Dreller, 1993; Dreller and Kirchner, 1994), similar in function and form to what is produced in A. mellifera (Kirchner et al., 1988). Interestingly, the other giant honey bee A. laboriosa, which does not forage nocturnally, is evidently silent (Kirchner et al., 1996; Oldroyd and Wongsiri, 2006). This absence of an acoustical component provides further support for the hypothesis that the waggle run buzz is an adaptation for dancing in the dark. What remains unknown is whether this acoustical addition was then lost in A. la-

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boriosa or if it were gained independently in several lineages (Kirchner et al., 1996; Oldroyd and Wongsiri, 2006). The Asian cavity nesters, of which Apis cerana is beststudied, are thought to be the most derived of the species. Like A. mellifera and A. dorsata, A. cerana dance relative to gravity and retain the addition of sound pulses. In fact, the dances of A. mellifera and A. cerana are similar enough that each attends and is recruited by the dance of the other (Tan et al., 2008), suggesting that the evolution of this dance form pre-dated this particular speciation event (Oldroyd and Wongsiri, 2006; Tan et al., 2008).

A future step in dance language biology The waggle dance remains a rich repository of challenges and questions to be answered. One reason for its prolic nature is that waggle dance research may focus on both basic and applied biology. In recent years, the honey bee has experienced a global decline (Aizen and Harder, 2009; Carreck and Neumann, 2010; Ratnieks and Carreck, 2010). The reasons behind this decline are complex and multi-faceted (Cox-Foster et al., 2007; Oldroyd, 2007), but one possible factor contributing to the problem could be that there is less available forage for the bees (Dhruba, 2009; Ratnieks and Carreck, 2010). Therefore, it is important to understand better where the bees are currently collecting their food. From von Frisch to current times, the waggle dance has been used to determine where bees forage (von Frisch, 1967; Visscher and Seeley, 1982; Waddington et al., 1994; Steffan-Dewenter and Kuhn, 2003). With the waggle dance, the bees themselves tell us where they nd resources. With advances in GIS and other tools used in landscape ecology, the dance language may be integrated into a research framework for applied honey bee conservation biology. Little things I saw on the side William Bateson, the biologist credited with bringing Mendel to the attention of the English-speaking world, counsels new scientists with this: Treasure your exceptions! When there are none, the work gets so dull that no one cares to carry it further. Keep them always uncovered and in sight. Exceptions are like the rough brickwork of a growing building which tells that there is more to come and shows where the next construction is to be, (Bateson, 1908). His words are particularly poignant in reference to dance language investigations, as one of the hallmarks shared by both von Frisch and Lindauer was the particular attention paid to unexpected behaviors or, as Lindauer put it, to the little things I saw on the side (Seeley et al., 2002). This curiosity, this ability to notice and to respond to the unex-

plained, directed not only current investigations, but also informed on future topics. In fact, probably most of the advances that have developed in the years since von Frisch have been the direct result of scientists noticing and investigating not a grand, theoretical topic (Seeley et al., 2002), but simply an unusual bee behavior. Is this phenomenon of noticing the little side things unique to honey bee biology? Not necessarilyscience of course requires the curiosity for the unexplained. However, unlike most Nobel Prizes, the waggle dance is a discovery that we are able to witness with the naked eye. In this way, anyone may watch and wonder at the intricate behaviors of a tiny insect. All that is necessary for initiation into, as von Frisch put it, magic well for discoveries, is the bee.
Acknowledgments I would like to thank Fiona Riddell Pearce, s Leo n Contrera, and James Nieh for ter, Felipe Andre Christoph Gru their helpful comments on this manuscript. I also thank two anonymous reviewers for their useful comments and suggestions. MJC is funded by The Nineveh Charitable Trust.

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