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Dyer, 2002. the Biology of the Dance Language 1 Nov 2001 11:4 AR AR147-29.tex AR147-29.SGM ARv2(2001/05/10) P1: GSR Annu. Rev. Entomol. 2002. 47:917–49 Copyright c 2002 by Annual Reviews. All rights reserved THE BIOLOGY OF THE DANCE LANGUAGE Fred C. Dyer Department of Zoology, Michigan State University, East Lansing, Michigan 48824; e-mail: [email protected] Key Words Apis, honey bee, communication, navigation, behavioral evolution, social organization ■ Abstract Honey bee foragers dance to communicate the spatial location of food and other resources to their nestmates. This remarkable communication system has long served as an important model system for studying mechanisms and evolution of complex behavior. I provide a broad synthesis of recent research on dance commu- nication, concentrating on the areas that are currently the focus of active research. Specific issues considered are as follows: (a) the sensory and integrative mechanisms underlying the processing of spatial information in dance communication, (b) the role of dance communication in regulating the recruitment of workers to resources in the environment, (c) the evolution of the dance language, and (d ) the adaptive fine-tuning of the dance for efficient spatial communication. CONTENTS INTRODUCTION .....................................................918 THE DANCE AS A SPATIAL COMMUNICATION SYSTEM .................918 SPATIAL-INFORMATION PROCESSING IN DANCE COMMUNICATION ..................................................921 Measurement of Distance .............................................922 Measurement of Direction: The Celestial Compass .........................923 Dance Orientation: Coding Flight Direction into Dances .....................925 Distance Signal: Coding Flight Distance into Dances .......................926 Information Transfer from Dancer to Follower .............................927 Does the Waggle Dance Communicate Height? ............................930 DANCE COMMUNICATION AND DECISION MAKING BY COLONIES ......................................................930 EVOLUTIONARY ORIGIN OF THE DANCE LANGUAGE ...................932 Origins: Insights from the Genus Apis ...................................933 Origins: Insights from Other Social Bees .................................936 ADAPTIVE DESIGN OF DANCES FOR EFFICIENT SPATIAL COMMUNICATION .........................................938 Distance Dialects ....................................................938 Tuned Error in the Divergence Angle ....................................940 Migration Dances ....................................................941 FUTURE DIRECTIONS ................................................942 0066-4170/02/0101-0917$14.00 917 1 Nov 2001 11:4 AR AR147-29.tex AR147-29.SGM ARv2(2001/05/10) P1: GSR 918 DYER INTRODUCTION More than a half century ago, Karl von Frisch put forth the astonishing hypothesis that honey bees (genus Apis) communicate the location of food and other resources through body movements he called dances. These dances, done by foragers on their return to the nest, had been described by many observers over several centuries and had long been assumed to play some role in communication about food. Von Frisch’s realization that dances carry spatial information was surely one of the major discoveries in behavioral biology in the twentieth century. Along with discoveries by other ethologists such as Lorenz and Tinbergen, the elucidation of the dance language opened our eyes to the sophistication and complexity of animal behavior and helped establish the study of behavior as a rigorous empirical science. Furthermore, experimental studies of dance language have provided a window to the subjective world, or Umwelt (115), of the honey bee. This window has provided an unusually clear view not only of what it is like to be a bee, but more generally of what it is like to be an insect. In the 1960s, von Frisch published a masterly review of research on the dance language by him and his students (116a). Since that book’s publication, work on the dance language has been pursued vigorously, leading to a greatly expanded under- standing of the sensory basis of dance communication, the role of the dance in the foraging strategy of the honey bee colony, and the evolution of this remarkable be- havior. Reviews of this more recent research have generally focused on one or a few aspects of the dance language (19, 38, 40, 41, 58, 66, 97). I adopt a broad, synthetic approach to convey the full range of questions that are addressed by research on the dance language and to review major recent developments and current frontiers. My review relies most heavily on studies of the several races of the western hive bee Apis mellifera, which is the species von Frisch studied and is still widely used as a model organism. However, I also incorporate insights from studies of other species of Apis, all of which live in Asia (87, 104). These species share a number of traits with A. mellifera, including highly eusocial colonies, the construction of a wax comb in which brood are reared and food is stored, and communication based on dances. However they also exhibit striking differences in body size, colony size, nest architecture, and properties of the dances. Study of these differences has exposed new insights into both the mechanisms and evolution of the dance (19). THE DANCE AS A SPATIAL COMMUNICATION SYSTEM In a typical instance of dance communication (116a), a successful forager returns home from a rich food source and is greeted by other workers who, if she is carrying nectar, induce her to regurgitate her load to them. If this welcome is enthusiastic enough, the forager begins dancing on the vertical sheet of comb. The dance consists of a series of repeated waggling runs in which the bee moves in a particular direction along the comb while waggling her body from side to side. 1 Nov 2001 11:4 AR AR147-29.tex AR147-29.SGM ARv2(2001/05/10) P1: GSR HONEY BEE DANCE LANGUAGE 919 During the waggling run she also emits a burst of sound by buzzing her wings. After each waggling run, the dancer circles around and realigns herself to begin the next waggling run. As the bee dances, she is encircled by 1–6 other bees that face toward the dancer and follow her movements. The dance followers observe several waggling runs and then leave the nest. Many of these eventually reach the same feeding place that the dancer had found or a feeding place close by. The orientation of the waggling run and its duration are highly correlated with the direction and distance that the forager has flown to the food (Figure 1). Speci- fically the angle of the waggling run relative to the upward direction on the comb Figure 1 Waggle dance of honey bees (Modified from 92). During the flight to food or another resource, honey bees measure the direction (relative to the sun) and distance to the food. Direction is encoded in the orientation of the waggling run relative to gravity (or relative to the sun if celestial cues are visible during the dance). Distance is encoded in the duration of the waggling run. Different populations have different functions relating flight distance to waggling run duration. Other bees observing the dance use the spatial information it contains to fly to the general location of the food and odors carried by the dancer to pinpoint the actual resource. 1 Nov 2001 11:4 AR AR147-29.tex AR147-29.SGM ARv2(2001/05/10) P1: GSR 920 DYER correlates with the direction of flight relative to the sun and sun-linked patterns of polarized sky light. Dancers may also be oriented to these celestial cues directly if they can see them (e.g., when they are dancing on the surface of a reproductive swarm). The duration of the waggling run increases monotonically with flight distance, as can be observed in dances of bees trained to feeders at known flight distances. By placing arrays of feeders or baits in the environment, von Frisch found that recruits searched preferentially at baits near the one being visited by the dancer, suggesting that they had found their way there by using spatial information obtained from the dance. Von Frisch also described another form of the dance that he called a round dance because the bee circled repeatedly in place, occasionally changing the direction of turning. This type of dance is done by bees that have flown to locations near the nest. Von Frisch suggested that round dances signal recruits to search near the nest, but they convey no information about direction. More recent research has revealed that many round dances actually contain directional information (56). Dancers produce sounds during round dances, when their bodies are aligned in the direction corresponding to that of the food. Thus, round dances may best be interpreted as waggle dances with short-distance signals. On the other hand, recruits that have followed round dances search in all directions near the nest (116a), thus they may have difficulty obtaining directional information from such dances. Von Frisch emphasized an important role for odors in the recruitment process. Specifically, he suggested that floral odors and other environmental chemicals cling to the body of the foragers and are detected by the dance followers. Foragers also release an attractive pheromone on their return to a familiar feeding place. The spatial information in the dance allows recruits to get only to the general vicinity of the food; odors allow them to pinpoint the resource indicated by the dancer (116a). A powerful source of odors can even lead recruits to ignore the spatial information in the
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