House hunting by honey bees a study of

House hunting by honey bees a study of group decision making Thomas D. Seeley Department of Neurobiology and Behavior Cornell University

The question of social choice: How can a group use the knowledge and opinions possessed by its members to produce an optimal choice of action for the group as a whole? Group decision making Individual Inputs Aggregation Process Group Action

A Swarm of Bees • One queen bee • ~ 10, 000 worker bees • 3 -5% are active (300 -500 scout bees) • 95 -97% are quiescent

Home Sweet Home

Pioneering discovery by Martin Lindauer: scout bees report potential home sites with waggle dances (1955) Martin Lindauer Karl von Frisch

Coding location information in waggle dance 1. Angle of waggle run indicates direction. 2. Duration of waggle run indicates distance.

Lindauer’s key findings • Initially, bees perform dances for multiple sites • Before swarm flies away, all dances indicate one site • The swarm flies to the consensus site, moves in • Therefore, dances on swarm indicate nest sites • Scouts are holding a kind of plebiscite on the swarm’s new home Lindauer (1955) Z. vergl. Physiol. 37: 263 -324.

The real estate preferences of bees (1975) • • • (“>” means “is preferred to”) Entrance height: 5 > 1 m Entrance area: 15 > 75 sq cm Entrance direction: south > north Entrance position: bottom > top Cavity volume: 40 > 10 liters Combs: with > without

How does social choice (democracy) work in a honey bee swarm? How exactly do the scout bees conduct their group decision making?

Detailed eavesdropping on the scout bees’ “debate” on a swarm

One 16 -hour “debate”: 11 sites, 149 scouts Seeley& Buhrman (1999) Behav. Ecol. Sociobiol. 45: 19 -31.

Decision-making process: consensus building or quorum sensing? Dancer consensus at swarm? Scout quorum at site? What is the decision evidence? Where is it accumulating?

Laboratory for experiments with house hunting bees: Appledore Island, Maine (Shoals Marine Laboratory, Cornell University)

Testing the hypothesis of quorum sensing Critical prediction: Delaying quorum formation at the chosen site, while leaving the rest of the decision-making process undisturbed, should delay the reaching of a decision.

Experimental methods Each swarm conducted its decision-making process twice, once with 1 nest box, and once with 5 nest boxes (or vice-versa).

1 nest-box trials vs. 5 nest-box trials 14: 00 15: 00 16: 00 7: 00 8: 00 9: 00 10: 00 11: 00 Seeley & Visscher (2004) Behav. Ecol. Sociobiol. 56: 594 -601. • Slower buildup of scouts at each nest box • No decrease in dancing at swarm • Marked delay in time to decision! (on average, 3. 3 vs 7. 4 hours, P < 0. 005)

Conclusions • Decision evidence: number of scouts at each site • Making a decision: accumulating a threshold number (quorum) of bees at a site • How bees sense the quorum remains a mystery

Decision making by accumulation of evidence Monkey brain Bee swarm Selected nest box quorum Nonselected nest box

When quorum is reached, scout bees produce an acoustical signal (“worker piping”) to stimulate non-scouts to warm up for flight Seeley & Tautz (2001)

Piping/warming takes 30 -60+ minutes Seeley, Kleinhenz, Bujok &Tautz (2003) Naturwissenschaften 90: 256 -260. Why quorum sensing, not consensus sensing? Warm up starts as soon as enough scouts (not all scouts) have approved of a site: boost speed, maintain accuracy

Does a swarm choose the best of the various sites that it examines?

Variable quality nest site

Scouts visible at nest box Results (note: winner takes all) Time of day Seeley & Buhrman (2001) Behav. Ecol. Sociobiol. 49: 41416 -427.

What are the behavioral processes of the individual scout bees that underlie the rapid buildup of scouts at superior sites, and the eventual decline of scouts at the inferior ones?

“Friendly competition” among coalitions of committed scouts for the uncommitted scouts So-so site Superb site Site 1 r 1 Uncommitted r 2 Site 2 bees a 1 Scout bees a 2 bees N 1 U For each site i: d. Ni/dt = Niri. U - Niai Bees need this: r 1 > r 2 and a 1 < a 2 N 2

Tuning of dance duration as a function of site quality Seeley & Buhrman (2001) Behav. Ecol. Sociobiol. 49: 41416 -427.

A bee makes multiple visits to her site, but dances less and less strongly after each visit (phasic, not tonic, coding of site quality) Seeley (2003) Behav. Ecol. Sociobiol. 53: 417 -424.

Decay function for scout’s nest-site dances 6 5 4 3 2 1 0 Remaining returns to swarm with dancing Seeley (2003) Behav. Ecol. Sociobiol. 53: 417 -424.

Why the scout buildup is strongest at the best site Superb site 90+75+60+45+30+15 = 315 waggle runs So-so site 30+15 = 45 waggle runs 6 5 4 3 2 1 0 Remaining returns to swarm with dancing • Scouts for the best site have the highest per capita recruitment (“birth”) rate and the lowest per capita abandonment (“death”) rate. • Population of scouts for the best site grows most rapidly, and ultimately overwhelms, all populations for other sites.

Dynamics on swarm cluster and at nest sites that underlie swarm decision making Seeley, Visscher & Passino (2006) Amer. Scientist 94: 220 -229.

Good decision making by groups is not automatic “The mass never comes up to the standard of its best member, but on the contrary degrades itself to a level with the lowest. ” —Henry David Thoreau, Journal, 14 March 1838 “Madness is the exception in individuals but the rule in groups. ” —Friedrich Nietzsche, Beyond good and evil, 1886

Swarm Smarts! 1. Promote diversity of knowledge within 2. the group –scouts search autonomously and report freely 2. Avoid tendency to conformity, rapid consensus –scouts conduct an open competition among opinions –scouts assess and report sites independently 3. Aggregate opinions with both speed and accuracy –scouts use quorum sensing, with moderate quorums

Collaborators Brigitte Bujok (Würzburg) Susannah Buhrman (Cornell) Marco Kleinhenz (Würzburg) Roger A. Morse (Cornell) Kevin Passino (Ohio State) Jürgen Tautz (Würzburg) Kirk Visscher (UC-Riverside) Field Assistants Siobhan Cully Robert Fathke Benjamin Land Adrian Reich Ethan Wolfson-Seeley Funding Inspiration National Science Foundation Martin Lindauer (Würzburg) National Geographic Society U. S. Dept. of Agriculture