The Honey Bee Dance Language Amy Toth March 1, 2007

Symbolic Communication Communication of environmental information that has been coded and transmitted to a receiver “Most sophisticated” form of animal communication - James Nieh Practiced by: –Humans (verbal language, etc.) –Some Great Apes –Honey bees!

For honey bees, finding nectar is essential to survival.

Aristotle, B.C.E. Historia Animalium (330 B.C.E.) Bees recruit others to specific food source Observed bees making “dancing” movements

Karl von Frisch, Austrian, began work in 1919 Trained European honey bees, Apis mellifera, to feeders First believed bees used flower scents or other odors to find food sources Began to pay close attention to dances performed by returning foragers –Dances very precise, with varying tempo and direction

von Frisch described the dances 1. “Round dance” When food source is < 50 m from hive

2. “Waggle dance” When food source is > 50 meters away Waggle run - Abdomen wagging and wing fluttering -Angle repeated with respect to vertical, or gravity (here 20° right)

angle b/w vertical & waggle run = angle b/w sun & food source “Waggle dance” Figure-8 portion resets position of dancer

And that’s not all… By moving feeder to different angles and locations, von Frisch found: Number of waggles per run correlates with distance to food source (more= farther) Dance “tempo” (slower= farther) The duration of the dance (longer= better food) Other bees follow the dancer (“audience”) SCOUT: finds new food sources & dances RECRUITS: follow dances & then forage

PLUS! Short stops in which the dancer doles out samples of the food to her audience  Taste and smell of the food!

In summary, von Frisch was proposing the waggle dance says… 1) DIRECTION: - Angle of waggle run 2) DISTANCE: - Number of waggles per run - Dance tempo (# of circuits per unit time) 3) QUALITY: - The duration of the dance (total waggle runs) 4) TASTE AND SMELL: -Dancer gives free samples *** ROUND DANCE- only for nearby sources, detailed info not provided

Questioning von Frisch…

von Frisch’s Experimental Evidence DIRECTION Train foragers to feeding station F. Then, collect new recruits to all feeding stations (equidistant, controlled for food quality).

DISTANCE: Train foragers to come to a feeding station 750 meters from the hive. Look at number of recruits to stations at various distances (same direction, controlled for food quality)

Vertical combs necessary: gravity reference needed for dance to work Horizontal combs: disoriented dances Vertical combs: oriented dances Von Frisch, 1967

Objections… Adrian Wenner, 1967 Olfactory map hypothesis: Bees use smells and tastes from returning foragers to locate food sources When odor carried by forager provided at all plates, bees’ preference disappeared

The Nobel Prize in Physiology or Medicine 1973 “for their discoveries concerning organization and elicitation of individual and social behavior patterns” Karl von Frisch for decoding the bee dance language Shared with Konrad Lorenz and Niko Tinbergen Only Nobel Prize for animal behavior (so far)

That same year… Do Honey Bees have a Language? Nature - January, Pages PATRICK H. WELLS & ADRIAN M. WENNER University of California, Santa Barbara, CA Von Frisch and later adherents of the theory that honey bees communicate by means of an elaborate dance are challenged by controlled experiments which show that their data can be explained in terms of olfactory cues.

Unquestionable evidence, Gould 1975 Make a scout “lie”, and dance about a source she has never visited This would provide incontrovertible proof that information is contained in the dances

A Clever Experiment Ocelli: simple eyes that perceive light intensity If a bright light is placed above the hive, bees will orient their dances with respect to the light instead of with respect to gravity If ocelli covered, bees less sensitive, do not reorient dances ** Idea: ocelli-covered dancers will “misdirect” recruits with uncovered ocelli

Gould’s experiment To ocelli-untreated recruits, station specified by dancing, 90º to right of sun x What light? Food straight ahead, girls! Ooh, pretty light. Must be the sun. Dancer says “food 90º to right of sun.” **If recruits follow odor, should arrive at odor-marked forager station  no! ** If recruits follow dance, should arrive at location specified by dance  yes, with little error! Hive odor Forager stn. Recruit Stns.

The controversy subsides The dance language communicates information about location and quality of food source Odors probably do affect the speed and accuracy of recruits Wenner becomes a marine biologist "Throughout the dance-language controversy, Wenner has made perceptive and valuable contributions. Von Frisch's controls do not exclude the possibility of olfactory recruitment alone" -- Gould

Evolutionary Basis of Bee Dances (Lindauer) Comparative studies with existing, related social bees Another honey bee, Apis florea –Horizontal dances –Orient waggle run directly at food source (pointing) –Less sophisticated form of dance? Apis florea nest

Stingless bees Various species exhibit forms of recruitment to food sources Can these provide hints to the steps involved in dance language evolution? Apis and Trigona

1. “Simple”, some Trigona stingless bees –Foragers arouse nestmates with high-pitched buzzing sounds –Foragers carry floral odor –Nestmates leave in search of same floral odor 2. “Intermediate”, other Trigona species –Pheromone marking by forager: at foraging site and on the trail –At nest, forager makes buzzing sounds to attract recruits –Recruits follow forager back to the site, guided by pheromones Trigona carbonaria forager

3. “More advanced”, Melipona stingless bees A) DIRECTION: Forager does a short zig-zag flight in direction of food source (incomplete leading) B) DISTANCE: Pulses of sound produced while “dancing” (longer pulses, farther food) (Nieh)

C) HEIGHT: Sounds made while unloading food inform recruits of height of food (Nieh) Symbolic communication likely, but not completely confirmed for stingless bees.

But, phylogenetic perspective differs from Lindauer’s story Family Apidae Molecular phylogeny suggests stingless bees are NOT closely related to honey bees (Cameron & Mardulyn) Honey bees Stingless bees Recruitment systems in these social bees may therefore have evolved totally independently!

Adaptive Value of the Dance 1) Saves time? -- NO, recruits take just as long as scouts to find a foraging source 2) Allows recruits to monopolize rewarding food sources? -- YES 3) Especially important in patchy, complex environments (Sherman & Visscher)  Allows bees to quickly exploit resources, before their discovery by other colonies (Seeley & Visscher)

Much ongoing work…

How do bees follow a dance in the dark hive? Wing vibrations produce a sound (strong air-particle oscillations) Bees with clipped wings ineffective dancers Robo-bee!!! –Produced bee dance movements –If razor blade wings did not vibrate, dance ineffective (Kirchner & Towne)

How do bees measure distance? Von Frisch suggested energy burned during flight signaled bees the distance flown Instead, bees use “optic flow” of landscape to measure distance (Esch, Srinivasan & colleagues)

Do recruits make a “bee line” to food? Harmonic radar “waggle dance controversy resolved”

Other dances –Waggle dance used during swarming to communicate possible nest sites –“Grooming dance”– elicits nestmates to help a bee groom –“Buzzing runs” used to elicit swarming behavior (Land & Seeley)

Honey bee dance language Demonstration of complex, cognitively demanding communication in an insect! Communication systems of other insects (e.g., stingless bees) likely as complex Elegant experimental work

Have a great weekend!