Honeybee Democracy - Thomas D. Seeley (2010)

Notes

Chapter 1. Introduction

Page 3: Quote of George Bernard Shaw, from Shaw, G. B. 1903. Man and Superman. Act II, line 79. The University Press, Cambridge, MA.

Page 3: The scope and economic value of honeybee pollination is reviewed in detail in two classic works. McGregor, S. E. 1976. Insect Pollination of Cultivated Crop Plants. Agricultural Handbook 496. United States Department of Agriculture, Agricultural Research Service, Washington DC; and Free, J. B. 1993. Insect Pollination of Crops. Academic Press, London.

Page 3: Bee taxonomists tell us that there are at least nine species of honeybees, all members of the genus Apis. The biology and geographic distribution of each species, including the familiar western honeybee, Apis mellifera, are described in detail in Ruttner, F. 1988. Biogeography and Taxonomy of Honeybees. Springer-Verlag, Berlin. A recent paper updates what is known about the living and fossil honeybees (genus Apis), and discusses the biogeography of these bees given the remarkable discovery recently of a fossil honeybee (Apis nearctica) recovered from paper shales of Nevada in the western United States. See Engel, M. S., I. A. Hinojosa-Diaz, and A. Rasnitsyn. 2009. A honey bee from the Miocene of Nevada and the biogeography of Apis (Hymenoptera: Apidae: Apini). Proceedings of the California Academy of Sciences 60:23–38.

Page 5: A good review of studies on the queen honeybee’s pheromonal infuence on her workers is provided by Winston, M. L., and K. N. Slessor. 1992. The essence of royalty: honey bee queen pheromone. American Scientist 80:374–385.

Page 6: The analogy between the bees in a hive and the cells in a body—in both cases, a constellation of units at one level of biological organization cooperate closely to build a higher level entity—is discussed in detail in Hölldobler, B., and E. O. Wilson. 2009. The Superorganism:The Beauty Elegance, and Strangeness of Insect Societies. Norton, New York.

Pages 7–8: The study of the neurobiology of primate decision making has made its most striking progress in understanding how simple perceptual decisions are made, that is, how an individual’s nervous system transforms sensory information into a perception and then into an appropriate behavioral response. Two recent reviews of this field of study are Gold, J. I., and M. N. Shadlen. 2007. The neural basis of decision making. Annual Review of Neuroscience 30:535–574; and Heekeren, H. R., S. Marrett, and L. G. Ungerleider. 2008. The neural systems that mediate human perceptual decision making. Nature Reviews Neuroscience 9:467–479.

Page 8: Quote of Henry David Thoreau, from Thoreau, H. D. 1838. Journal entry, March 14.

Page 8: Quote of Friedrich Nietzsche, from Nietzsche, F. 1966. Beyond Good and Evil. Random House, New York. Kaufmann, W., trans. 1886. Jenseits von Gut und Böse. P. 90. Naumann, Leipzig.

Pages 9–11: A clear description of how Karl von Frisch gradually decoded the waggle dance is found in chapter 3 of von Frisch, K. 1971. Bees: Their Vision, Chemical Senses, and Language. Cornell University Press, Ithaca, NY. The definitive report of von Frisch’s experimental analysis of this communication system is von Frisch, K. 1993. The Dance Language and Orientation of Bees. Harvard University Press, Cambridge, MA. A recent confirmation of his conclusion that bees share information about rich food sources by means of waggle dances is Riley, J. R., U. Greggers, A. D. Smith, D. R. Reynolds, and R. Menzel. 2005. The flight paths of honeybees recruited by the waggle dance. Nature 435:205–207.

Page 9: Quote of Karl von Frisch, from von Frisch, K. 1954. The Dancing Bees:An Account of the Life and Senses of the Honey Bee. Methuen, London. Pp. 101, 103.

Page 12: For detailed biographical information on Martin Lindauer, see Seeley, T D., S. Kühnholz, and R. H. Seeley. 2002. An early chapter in behavioral physiology and sociobiology: the science of Martin Lindauer. Journal of Comparative Physiology A 188:439–453.

Page 13: Quote of Martin Lindauer regarding world of humanity, from Seeley, T D., S. Kühnholz, and R. H. Seeley. 2002. An early chapter in behavioral physiology and sociobiology: the science of Martin Lindauer. Journal of Comparative Physiology A 188:439–45 3. P. 442.

Page 13: Quote of Martin Lindauer regarding beautiful experience, from Seeley, T D, S. Kühnholz, and R. H. Seeley. 2002. An early chapter in behavioral physiology and sociobiology: the science of Martin Lindauer. Journal of Comparative Physiology A 188:439–453. P. 447.

Page 14: Quote of Martin Lindauer regarding dirty dancers, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 266. Translated by T D. Seeley.

Pages 14–16: Lindauer’s discovery that bees can use waggle dances to announce nest sites as well as food sources was first reported in Lindauer, M. 1951. Bienentänze in der Schwarmtraube. Die Naturwissenschaften 38:509–513.

Page 17: Roger A. Morse served as professor of apiculture at Cornell University for 40 years, from 1957 to 1997. He supervised the studies of over 30 graduate and postdoctoral students and wrote many leading books on beekeeping, including The Complete Guide to Beekeeping (1972, Dutton, New York) and Bees and Beekeeping (1975, Cornell University Press, Ithaca, NY).

Page 17: See Wilson, E. O. 1971. The Insect Societies. Harvard University Press, Cambridge, MA.

Page 18: See Lindauer, M. 1961. Communication among Social Bees. Harvard University Press, Cambridge, MA.

Page 18: Lindauer’s magnum opus on house hunting by honeybees is Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. An English translation, titled House-hunting by honey bee swarms, exists as a supplement to Visscher, P. K. 2007. Group decision making in nest-site selection among social insects. Annual Review of Entomology 52:255–275. It is available online at http://arjournals.annualreviews.org/toc/ento/52/1.

Chapter 2. Life in a Honeybee Colony

Page 20: Quote of Charles Butler, from Butler, C. 1609. The Feminine Monarchie: Or, A Treatise concerning Bees and the Divine Ordering of Them. Preface, p. 4. Joseph Barnes, Oxford.

Page 20: The most comprehensive “Who’s Who” of bees is Michener, C. D. 2000. The Bees of the World. Johns Hopkins University Press, Baltimore. For a detailed and beautifully illustrated review of the evolutionary history of bees, see chapter 11, Hymenoptera: ants, bees, and other wasps, in Grimaldi, D., and M. S. Engel. 2005. Evolution of the Insects. Cambridge University Press, Cambridge. The recent discovery of the oldest known fossil bee is reported in Poinar, G. O., Jr., and B. N. Danforth. 2006. A fossil bee from Early Cretaceous Burmese amber. Science 314:614.

Page 21: The complex mutualism between flowering plants and bees is reviewed in Proctor, M., P. Yeo, and A. Lack. 1996. The Natural History of Pollination. Timber Press, Portland, OR. See also Barth, F. G. 1985. Insects and Flowers: The Biology of a Partnership. Princeton University Press, Princeton, NJ.

Page 21: The biology of solitary bees is reviewed in comparison to the biology of social bees in Michener, C. D. 1974. The Social Behavior of the Bees. Harvard University Press, Cambridge, MA.

Page 21: An observation hive for honeybees is one in which a colony of bees lives between two panes of glass. The hive is built like a sandwich, with the glass for bread and the bees’ double-sided comb as filling in the middle. There is a space beneath the glass on each side of the comb so that a single layer of bees can walk around on the comb. Thus all of the hive’s inhabitants are always exposed, and a person can peer easily into their normally private world.

Pages 21–25: The anatomy and reproductive biology of workers, queens, and drones are described in detail in Winston, M. L. 1987. The Biology of the Honey Bee. Harvard University Press, Cambridge, MA. For an utterly gorgeous description of bee anatomy—with magnificent photographs, micrographs, drawings, and paintings—see Goodman, L. 2003. Form and Function in the Honey Bee. International Bee Research Association, Cardiff.

Page 25: The concept of a honeybee colony as a superorganism is developed in Seeley, T. D. 1989. The honey bee colony as a superorganism. American Scientist 77:546–553. For a detailed review of the biology of honeybees, with emphasis on how a colony functions as a unified whole, see Moritz, R.F.A., and E. E. Southwick. 1992. Bees as Superorganisms:An Evolutionary Reality. Springer-Verlag, Berlin. For a beautiful overview of insect (ant, termite, bee, and wasp) superorganisms, see Hölldobler, B., and E. O. Wilson. 2009. The Superorganism: The Beauty Elegance, and Strangeness of Insect Societies. Norton, New York.

Pages 25–27: For more detailed information on the topics of colony physiology mentioned here, see the following references. Thermoregulation: chapter 16, Social thermoregulation, in Heinrich, B. 1993. The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation. Harvard University Press, Cambridge, MA. Carbon dioxide regulation: Seeley, T D. 1974. Atmospheric carbon dioxide regulation in honey bee (Apis mellifera) colonies. Journal of Insect Physiology 20:2301–2305. Circulation of food: Basile, R., C.W.W. Pirk, and J. Tautz. 2008. Trophallactic activities in the honeybee brood nest—heaters get supplied with high performance fuel. Zoology 111:433–441. Fever response: Starks, P. T, C. A. Blackie, and T. D. Seeley. 2000. Fever in honey bee colonies. Naturwissenschaften 87:229–231.

Pages 27–33: The annual cycle of honeybee colonies is discussed more thoroughly in chapter 4, The annual cycle of colonies, in Seeley, T D. 1985. Honeybee Ecology. Princeton University Press, Princeton, NJ. See also Seeley, T D., and P. K. Visscher. 1985. Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecological Entomology 10:81–88.

Pages 33–34: The complexities of reproduction by honeybee colonies are described in greater detail in chapter 5, Reproduction, in Seeley, T D. 1985. Honeybee Ecology. Princeton University Press, Princeton, NJ, and in chapter 12, Drones, queens, and mating, in Winston, M. L. 1987. The Biology of the Honey Bee. Harvard University Press, Cambridge, MA.

Page 35: The three-year study of the survival, lifespan, reproductive rate, and other demographic characteristics of feral honeybee colonies, is reported in Seeley, T D. 1978. Life history strategy of the honey bee, Apis mellifera. Oecologia 32:109–118. An experimental test of the importance of swarming early in the summer is reported in Seeley, T D., and P. K. Visscher. 1985. Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecological Entomology 10:81–88.

Pages 35–42: For a detailed review of the process of honeybee swarming, see chapter 11, Reproduction: swarming and supersedure, in Winston, M. L. 1987. The Biology of the Honey Bee. Harvard University Press, Cambridge, MA.

Page 37: For more information about the curious shaking of the mother queen before her departure in a swarm, and her remarkably effective slimming regime, see Allen, M. D. 1959. The occurrence and possible significance of the “shaking” of honeybee queens by the workers. Animal Behaviour 7:66–69; and Pierce, A. L., L. A. Lewis, and S. S. Schneider. 2007. The use of the vibrational signal and worker piping to influence queen behavior during swarming in honey bees, Apis mellifera. Ethology 113:267–275. Note: the shaking signal is sometimes called the vibration signal or, more awkwardly, the “DVAV,” which stands for dorso-ventral abdominal vibration.

Pages 37–38: The first study that documented how worker bees become engorged with honey in preparation for swarming is Combs, G. F., Jr. 1972. The engorgement of swarming worker honeybees. Journal of Apicultural Research 11:121–128. More detailed reports on this phenomenon are provided by Otis, G. W., M. L. Winston, and O. R. Taylor, Jr. 1981. Engorgement and dispersal of Africanized honeybee swarms. Journal of Apicultural Research 20:3–12; and by Leta, M. A., C. Gilbert, and R. A. Morse. 1996. Levels of hemolymph sugars and body glycogen of honeybees (Apis mellifera L.) from colonies preparing to swarm. Journal of Insect Physiology 42:239–245. The structure of the wax glands and the physiology of beeswax production are reviewed in chapter 8, Glands: chemical communication and wax production, in Goodman, L. 2003. Form and Function in the Honey Bee. International Bee Research Association, Cardiff, and in Hepburn, H. R. 1986. Honeybees and Wax. Springer-Verlag, Heidelberg.

Page 38: “The calm before the swarm” is a quote of the worker bee Nyuki, from Hosler, J. 2000. Clan Apis. Active Synapse, Columbus, OH. P. 40.

Pages 38–39: For detailed reports on how the scout bees trigger the explosive departure of a swarm from its nest, see Rangel, J., and T D. Seeley. 2008. The signals initiating the mass exodus of a honeybee swarm from its nest. Animal Behaviour 76:1943–1952; Rangel, J., S. R. Griffin, and T D. Seeley, 2010. An oligarchy of nest-site scouts triggers a honeybee swarm’s departure from the hive. Behavioral Ecology and Sociobiology, in press. The two signals used by the scout bees—worker piping and buzz running—are described in two papers: Seeley, T. D., and J. Tautz. 2001. Worker piping in honey bee swarms and its role in preparing for liftof. Journal of Comparative Physiology A 187:667–676; and Rittschof, C. C., and T D. Seeley. 2007. The buzz-run: how honeybees signal “Time to go!” Animal Behaviour 75:189–197.

Page 40: The scent organ of worker honeybees, and the chemistry of its attraction pheromones, are reviewed in chapter 13, Attraction: Nasonov pheromone, in Free, J. B. 1987. Pheromones of Social Bees. Cornell University Press, Ithaca, NY.

Pages 40–42: For a detailed account of what happens to the virgin queens in a swarming colony after the primary swarm departs, see Gilley, D. C., and D. R. Tarpy. 2005. Three mechanisms of queen elimination in swarming honey bee colonies. Apidologie 36:461–474. For a thorough description of the behaviors of queens and workers when the virgin queens are having their flights to the death, see Gilley, D. C. 2001. The behavior of honey bees (Apis mellifera ligustica) during queen duels. Ethology 107:601–622. An analysis of the adaptive design of the flighting behavior of virgin queens is provided in Visscher, P. K. 1993. A theoretical analysis of individual interests and intracolony conflict during swarming of honey bee colonies. Journal of Theoretical Biology 165:191–212.

Page 41: The toots and quacks of queen honeybees are described precisely, based on laser vibrometer recordings, in Michelsen, A., W. H. Kirchner, B. B. Andersen, and M. Lindauer. 1986. The tooting and quacking vibration signals of honeybee queens: a quantitative analysis. Journal of Comparative Physiology A 158:605–611. For a general review of the diverse acoustical signals, both sounds and vibrations, that honeybees use in communicating in the darkness inside a hive, see Kirchner, W. H. 1993. Acoustical communication in honeybees. Apidologie 24:297–307.

Chapter 3. Dream Home for Honeybees

Page 43: Quote of Robert Frost, from “A Drumlin Woodchuck,” in Latham, E. C, ed. 1969. The Poetry of Robert Frost. Henry Holt, New York.

Pages 43–44: The history of mankind’s association with bees, as evidenced by material objects (cave paintings, illuminated manuscripts, hives and their shelters, and beekeeping tools), is explored in Crane, E. 1983. The Archaeology of Beekeeping. Duckworth, London.

Page 45: The first experimental studies of the nest-site preferences of honeybees are reported in Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für verglei-chende Physiologie 37:263–324. An English translation, titled House-hunting by honey bee swarms, exists as a supplement to Visscher, P. K. 2007. Group decision making in nest-site selection among social insects. Annual Review of Entomology 52:255–275. It is available online at http://arjournals.annualreviews.org/toc/ento/52/1.

Page 45: Quote of Martin Lindauer about asking the bees themselves, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 290. Translated by P. K. Visscher.

Page 47: Quote about the von Frisch–Lindauer approach to animal behavior research from Hölldobler, B., and E. O. Wilson. 1994. Journey to the Ants. Harvard University Press, Cambridge, MA. P. 19.

Pages 49–51: For a detailed report on the nests of honeybees living in trees, see Seeley, T. D., and R. A. Morse. 1976. The nest of the honey bee (Apis mellifera L.). Insectes Sociaux 23:495–512.

Page 51: Forest beekeeping in medieval Russia, Poland, Germany, and England is reviewed in chapter 5, Forest “beekeeping” and the precursor of upright hives, in Crane, E. 1983. The Archaeology of Beekeeping. Duckworth, London. See also Galton, D. 1971. Survey of a Thousand Years of Beekeeping in Russia. Bee Research Association, London.

Page 52: The craft of lining bees is best described in Edgell, G. H. 1949. The Bee Hunter. Harvard University Press, Cambridge, MA. Edgell, who was director of the Museum of Fine Arts in Boston, had hunted bee trees in New Hampshire since his boyhood and once said that his book on bee hunting brought him greater fame than his professional publications on fine arts. I have used his no-nonsense methods for hunting wild colonies of bees in several ecological studies. See Visscher, P. K., and T. D. Seeley. 1982. Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63:1790–1801; Seeley, T. D. 2007. Honey bees of the Arnot Forest: a population of feral colonies persisting with Varroa destructor in the northeastern United States. Apidologie 38:19–29; and Seeley, T. D. 2008. The bees of the Arnot Forest. Bee Culture 136 (March):23–25.

Page 53: The use of bait hives in African beekeeping is described in Smith, F. G. 1960. Beekeeping in the Tropics. Longmans, London; and Guy, R. D. 1972. Commercial beekeeping with African bees. Bee World 53:14–22.

Pages 54–58: Full reports of my studies of the bees’ nest-site preferences are found in Seeley, T D. 1977. Measurement of nest cavity volume by the honey bee (Apis mellifera). Behavioral Ecology and Sociobiology 2:201–227; Seeley, T D., and R. A. Morse. 1978. Nest site selection by the honey bee Apis mellifera. Insectes Sociaux 25:323–337; and Visscher, P. K., R. A. Morse, and T D. Seeley. 1985. Honey bees choosing a home prefer previously occupied cavities. Insectes Sociaux 32:217–220. Other papers on the same topic include Jaycox, E. R., and S. G. Parise. 1980. Homesite selection by Italian honey bee swarms, Apis mellifera ligustica (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 53:171–178; Jaycox, E. R., and S. G. Parise. 1981. Homesite selection by swarms of black-bodied honey bees, Apis mellifera caucasica and A. m. carnica (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 54:697–703; and Rinderer, T E., K. W. Tucker, and A. M. Collins. 1982. Nest cavity selection by swarms of European and Africanized honeybees . Journal of Apicultural Research 21:98–103.

Page 55: The effects of entrance direction on the overwintering success of colonies is reported in Szabo, T I. 1983. Effects of various entrances and hive direction on outdoor wintering of honey bee colonies. American Bee Journal 123:47–49.

Page 56: The study of the size distribution of natural tree cavities in a Vermont forest is reported in Seeley, T D. 1977. Measurement of nest cavity volume by the honey bee (Apis mellifera). Behavioral Ecology and Sociobiology 2:201–227.

Page 57: The economics of comb construction are reviewed in chapter 6, Nest building, in Seeley, T D. 1985. Honeybee Ecology. Princeton University Press, Princeton, NJ.

Page 57: The extensive use of tree resins (“propolis”) by honeybees to seal their nesting cavities is described in Seeley T. D., and R. A. Morse. 1976. The nest of the honey bee (Apis mellifera L.). Insectes Sociaux 23:495–512. How the bees handle resins within the nest and how a colony controls its resin collection is reported in Nakamura, J., and T D. Seeley. 2006. The functional organization of resin work in honeybee colonies. Behavioral Ecology and Sociobiology 60:339–349.

Pages 58–59: The study of the Asian honeybees in Thailand is reported in Seeley, T D., R. H. Seeley, and P. Akratanakul. 1982. Colony defense strategies of the honeybees in Thailand. Ecological Monographs 52:43–63.

Page 59: For detailed information on the Yellow Rain story, see Seeley, T D., J. Nowicke, M. Meselson, J. Guillemin, and P. Akratanakul. 1985. Yellow rain. Scientific American 253 (September):128–137.

Page 59: KGB is the Russian acronym for the Committee of State Security (i.e., the national security agency) of the USSR. From 1954 to 1991, it was the communist state’s premier secret police and intelligence organization.

Page 60: For information on bait hives, see Morse, R. A. and T D. Seeley. 1978. Bait hives. Gleanings in Bee Culture 106 (May):218–220, 242; Morse, R. A., and T D. Seeley. 1979. New observations on bait hives. Gleanings in Bee Culture 107 (June):310–311, 327; Seeley, T. D., and R. A. Morse. 1982. Bait hives for honey bees. Cornell Cooperative Extension Information Bulletin No. 107; Witherell, P. C. 1985. A review of the scientific literature relating to honey bee bait hives and swarm attractants. American Bee Journal 125:823–829; Ratnieks, F.L.W. 1988. Improved bait hives. American Bee Journal 128:125–127; and Schmidt, J. O., S. C. Thoenes, and R. Hurley. 1989. Swarm traps. American Bee Journal 129:468–471.

Page 60: For information on attracting swarms to bait hives using attraction pheromones, see Free, J. B., J. A. Pickett, A. W. Ferguson, and M. C. Smith. 1981. Synthetic pheromones to attract honeybee (Apis mellifera) swarms. Journal of Agricultural Science 97:427–431; Schmidt, J. O., K. N. Slessor, and M. L. Winston. 1993. Roles of Nasonov and queen pheromones in attraction of honeybee swarms. Naturwissenschaften 80:573–575; Winston, M. L., K. N. Slessor, W. L. Rubink, and J. D. Villa. 1993. Enhancing pheromone lures to attract honey bee swarms. American Bee Journal133:58–60; and Schmidt, J. O. 1994. Attraction of reproductive honey bee swarms to artificial nests by Nasonov pheromone. Journal of Chemical Ecology 20:1053–1056.

Page 63: The character of the Isles of Shoals (Gulf of Maine) and the construction of the Shoals Marine Laboratory on Appledore Island in the 1960s and 1970s are described in Kingsbury, J. M. 1991. Here’s How We’ll Do It. Bullbrier Press, Ithaca, NY.

Pages 67–71: For a detailed report on the nest-site inspection behavior of scout bees and on the experimental analysis of how a small bee measures the volume of a large space, see Seeley, T. D. 1977. Measurement of nest cavity volume by the honey bee (Apis mellifera). Behavioral Ecology and Sociobiology 2:201-227.

Pages 71–72: The nifty algorithm, suggested by Nigel Franks and Anna Dornhaus, by which bees might measure the volumes of potential nesting cavities is described in Franks, N. R., and A. Dornhaus. 2003. How might individual honeybees measure massive volumes? Proceedings of the Royal Society of London B (Supplement) 270, S181–S182.

Chapter 4. Scout Bees’ Debate

Page 73: Quote of Jimmy Carter, from Carter, J. E. 1978. Address to the Parliament of India, June 2, 1978.

Pages 73–74: The New England town meeting is a fascinating form of small town democratic government. How it works is described in Mansbridge, J. J. 1983. Beyond Adversary Democracy. University of Chicago Press, Chicago; and Bryan, F. M. 2004. Real Democracy University of Chicago Press, Chicago.

Pages 75–84: The full report of Lindauer’s observations of dancing bees on swarm clusters is found in pages 265–282 in his magnum opus: Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. An English translation, titled House-hunting by honey bee swarms, exists as a supplement to Visscher, P. K. 2007. Group decision making in nest-site selection among social insects. Annual Review of Entomology 52:255–275. It is available online at http://arjournals.annualreviews.org/toc/ento/52/1.

Page 75: The phrase “watching and wondering” comes from the title of an autobiography written by Niko Tinbergen. See Tinbergen, N. 1985. Watching and wondering, in Dewsbury D. A., ed. Studying Animal Behavior: Autobiographies of the Founders. University of Chicago Press, Chicago. Pp. 431–46 3. Tinbergen strongly advocated starting a study of animal behavior by conducting a descriptive reconnaissance of the behavior to get a broad view of the phenomenon.

Page 76: The clever system devised by Karl von Frisch for making hundreds of bees individually identifiable using paint dots of just five colors is described in von Frisch, K. 1993. The Dance Language and Orientation of Bees. Harvard University Press, Cambridge, MA. Pp. 14–17.

Page 81: Quote of Martin Lindauer regarding a tug-of-war between two groups of dancers, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 276. Translated by P. K. Visscher.

Page 82: Lindauer describes two instances of a flying swarm making an emergency stopover while en route to its new home. See Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. Pp. 319–320.

Page 82: Quote of Martin Lindauer regarding a swarm dividing itself, from Lindauer, M. 1961. Communication among Social Bees. Harvard University Press, Cambridge, MA. P. 45.

Page 85: Quote of Martin Lindauer regarding scouts affiliated with losing sites giving up recruitment, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 275. Translated by P. K. Visscher.

Page 86: For a good discussion of the distinction between the two categories of group choice—consensus vs. combined—see Conradt, L., and T. J. Roper. 2005. Consensus decision making in animals. Trends in Ecology and Evolution 20:449–456; and Conradt, L., and C. List. 2009. Introduction. Group decisions in humans and animals: a survey. Philosophical Transactions of the Royal Society B 364:719-742.

Page 86: The full reference to the book mentioned here is Seeley, T D. 1995. The Wisdom of the Hive: The Social Physiology of Honey Bee Colonies. Harvard University Press, Cambridge, MA.

Pages 86–92: For the full report of the eavesdropping by Susannah Buhrman and me on the scout bees’ debates on three swarms, see Seeley, T D., and S. C. Buhrman. 1999. Group decision making in swarms of honey bees. Behavioral Ecology and Sociobiology 45:19–31.

Pages 93–94: Lindauer’s studies of which bees take up the profession of nest-site scout and when they do so are reported in Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. Pp. 296–307.

Page 94: Quote of Martin Lindauer regarding irresolute foragers, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 306. Translated by P. K. Visscher.

Pages 95–96: For a detailed report on Dave Gilley’s study of the striking age distribution of the nest-site scouts, see Gilley, D. C. 1998. The identity of nest-site scouts in honey bee swarms. Apidologie 29:229–240.

Page 96: For up-to-date discussions of how nature and nurture interact in shaping the complex social behavior of honeybees, see Robinson, G. E. 2004. Beyond nature and nurture. Science 304:397–399; and Robinson, G. E. 2006. Genes and social behaviour, in Lucas, J. R., and L. W Simmons, eds. Essays in Animal Behaviour: Celebrating 50 Years of Animal Behaviour. Elsevier, London. Pp. 101–113.

Pages 96–97: For the full report of Gene Robinson’s and Robert Page’s test for a genetic influence on a bee’s likelihood of becoming a nest-site scout, see Robinson, G. E., and R. E. Page, Jr. 1989. Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behavioral Ecology and Sociobiology 24:317–323.

Page 97: For a more detailed protocol for preparing artificial swarms, see the methods section in Seeley, T D. 2003. Consensus building during nest-site selection in honey bee swarms: the expiration of dissent. Behavioral Ecology and Sociobiology 53:417–424.

Page 98: Lindauer’s observations on what foragers were experiencing when they started scouting are reported in Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. Pp. 304–306.

Page 98: For detailed reports on how nectar foragers lose their enthusiasm for dancing and foraging when they have difficulty finding hive bees to take their nectar loads, see Seeley, T. D. 1989. Social foraging in honey bees: how nectar foragers assess their colony’s nutritional status. Behavioral Ecology and Sociobiology 24:181–199; and Seeley, T. D., and C. A. Tovey. 1994. Why search time to find a food-storer bee accurately indicates the relative rates of nectar collecting and nectar processing in honey bee colonies. Animal Behaviour 47:311–316.

Chapter 5. Agreement on Best Site

Page 99: Quote of John Milton, from Milton, J. 1671. Samson Agonistes. Line 1008.

Page 100: The economist Herbert A. Simon proposed the concept of bounded rationality in the mid 1950s in Simon, H. A. 1956. Rational choice and structure of environments. Psychological Review 63:129–138; and in Simon, H. A. Models of Man. Wiley, New York. For a recent book on the topic that includes several chapters on decision-making heuristics, see Gigerenzer, G., and R. Selten. 2001. Bounded Rationality: The Adaptive Toolbox. MIT Press, Cambridge, MA.

Page 100: A good discussion of one-reason decision making is provided by Gigerenzer, G., and D. G. Goldstein. 1999. Betting on one good reason: take the best and its relatives, in Gigerenzer, G., P. M. Todd, and The ABC Research Group, eds. Simple Heuristics That Make Us Smart. Oxford University Press, New York. Pp. 75–95.

Page 102: I believe that Susannah Buhrman and I observed a case of a first-rate site getting entered so late in a scout bees’ debate that the swarm rejected this excellent site in favor of a poorer one. This occurred when we watched the debate depicted in figure 4.6. Well into this debate, at 2:49 p.m. on June 20, the scout bee Green-White 39 landed on the swarm and in great excitement performed a lively and lengthy dance (166 dance circuits) for site L, just 200 meters (650 feet) to the southwest. She had discovered in a large white pine tree the empty nest of a wild colony that had died out over the preceding winter…a superb home! At 3:50 she again landed on the swarm and excitedly performed a second long-lasting dance (95 dance circuits). Meanwhile, however, dozens of other scouts were dancing rather faintheartedly for site I, 4,200 meters (13,800 feet, or 2.6 miles) to the south. Their dances contained on average only 6 dance circuits, indicating that site I was much less desirable than site L. Nevertheless, the swarm chose site I rather than site L, evidently because the excellent news brought back by Green-White 39 was too little and too late to redirect the swarm’s debate in favor of her superior alternative.

Page 102: The “secrets about the beautiful inner workings of a honeybee colony” that were uncovered at the Cranberry Lake Biological Station are described in Seeley, T. D. 1995. The Wisdom of the Hive. Harvard University Press, Cambridge, MA. This is a book worth reading!

Page 103–110: For the full report on the experiments that were conducted to determine how to create a mediocre, but acceptable, artificial nest site, see Seeley, T. D., and S. C. Buhrman. 2001. Nest-site selection in honey bees: how well do swarms implement the “Best-of-N” decision rule? Behavioral Ecology and Sociobiology 49:416–427.

Page 107: The specific procedure that we used for counting the number of scouts at a nest box was as follows. The person making the count sat 3 meters (about 10 feet) in front of the box and over a three-minute period made five counts of the maximum number of bees seen simultaneously at the box (either flying around it or crawling upon it) during a 30-second period. We used the average of these five counts as our measure of the scout bees’ interest in the box at that time.

Page 111: The evidence that the strength of a honeybee’s waggle dance provides an accurate readout of her evaluation of the desirability of a food source comes from several studies, including Waddington, K. D. 1982. Honey bee foraging profitability and round dance correlates. Journal of Comparative Physiology 148:297–301; Seeley, T D. 1994. Honey bee foragers as sensory units of their colonies. Behavioral Ecology and Sociobiology 34:51–62; and Seeley, T D., A. S. Mikheyev, and G. J. Pagano. 2000. Dancing bees tune both duration and rate of waggle-run production in relation to nectar-source profitability. Journal of Comparative Physiology A 186:813–819.

Pages 111–115: For the detailed description of the best-of-5 choice test, see Seeley, T D., and S. C. Buhrman. 2001. Nest-site selection in honey bees: how well do swarms implement the “Best-of-N” decision rule? Behavioral Ecology and Sociobiology 49:416–427.

Page 116–117: My study of honeybee colony survival as a function of nest cavity volume, which tests whether the bees’ nest-site preferences are beneficial to them, is not yet published. Some other studies that have likewise examined whether the nest-site preferences of animals enhance their reproductive success include Courtenay, S. C, and M.H.A. Keenleyside. 1983. Nest site selection by the fourspine stickleback, Apeltes quadracus (Mitchell). Canadian Journal of Zoology 61:1443–1447; Morse, D. H. 1985. Nests and nest-site selection of the crab spider Misumena vatia (Araneae, Thomisidae) on milkweed. Journal of Arachnology 13:383–390; Regehr, H. M., M. S. Rodway, and W. A. Montevecchi. 1998. Antipredator benefits of nest-site selection in black-legged kittiwakes. Canadian Journal of Zoology 76:910–913; and Wilson, D. S. 1998. Nest-site selection: microhabitat variation and its effects on the survival of turtle embryos. Ecology 79:1884–1892.

Chapter 6. Building a Consensus

Page 118: Quote from Society of Friends. 1934. Book of Discipline. Part I. Friends’ Book Centre, London.

Page 118–119: The recognition that democracy can come in two different forms— adversary and unitary—and that the mechanisms of decision making differ markedly between them, was first made in Mansbridge, J. J. 1983. Beyond Adversary Democracy. University of Chicago Press, Chicago. Mansbridge points out that the unitary process of decision making, unlike the adversary one, consists not in counting votes made by secret ballot to identify the majority opinion, but in an open and direct discussion to build a consensus. Clearly, the honeybee’s house-hunting process is an example of unitary democracy.

Pages 120–121: The analogy between the decision-making process of honeybee swarms and the democratic election process of our own societies was originally drawn in Britton, N. F., N. R. Franks, S. C. Pratt, and T. D. Seeley. 2002. Deciding on a new home: how do honeybees agree? Proceedings of the Royal Society of London B 269:1383–1388. The main aim of this paper was, however, to extend classical mathematical models of the spread of infectious diseases, and of infectious ideas, to elucidate the decision-making process of house-hunting honeybees. This theoretical work shows that there is no need for any bee to make comparisons between sites. Later empirical work (described later in this chapter) showed that indeed scout bees do not make comparisons of sites.

Pages 121–122: Lindauer’s observations on how a nest-site scout adjusts the strength of her dance according to the quality of the site she is advertising are reported in Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. Pp. 294–296.

Page 122: Quote of Martin Lindauer regarding lively versus lackluster dances, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 296. Translated by P. K. Visscher.

Page 123: The first quantitative evidence that scouts advertise superior nest sites with longer and livelier dances is reported in Seeley, T D., and S. C. Buhrman. 2001. Nest-site selection in honey bees: how well do swarms implement the “Best-of-N” decision rule? Behavioral Ecology and Sociobiology 49:416–427. The parallel finding that nectar foragers advertise richer flower patches by increasing the duration (= dance length) and rate (= dance liveliness) of dance-circuit production is reported in Seeley, T D., A. S. Mikheyev, and G. J. Pagano. 2000. Dancing bees tune both duration and rate of waggle-run production in relation to nectar-source profitability. Journal of Comparative Physiology A 186:813–819.

Page 123: Quote of Martin Lindauer regarding faint-hearted dance etc., from Lindauer, M. 1961. Communication among Social Bees. Harvard University Press, Cambridge, MA. P. 49.

Page 125–126: Kirk Visscher perfected the “abduction by aliens” method of labeling scout bees upon exiting a nest box when he performed some of the studies reported in Visscher, P. K. and S. Camazine. 1999. Collective decisions and cognition in bees. Nature 397:400.

Page 126–128: For the full report on how scouts behave differently when reporting on a high-quality (40-liter) nesting site versus a medium-quality (15-liter) one, see Seeley T. D., and P. K. Visscher. 2008. Sensory coding of nest-site value in honeybee swarms. Journal of Experimental Biology 211:3691–3697.

Page 129: A more complete analysis of how the problem of noisy individual-level coding of site quality decreases as the number of scouts reporting on a site increases is found in Seeley, T. D., and P. K. Visscher. 2008. Sensory coding of nest-site value in honeybee swarms. Journal of Experimental Biology 211:3691-3697.

Page 129: The handy expression “force of persuasion,” which is the product of the number of bees dancing for a site and the average number of dance circuits produced per dancing bee, comes from Britton, N. F., N. R. Franks, S. C. Pratt, and T. D. Seeley. 2002. Deciding on a new home: how do honeybees agree? Proceedings of the Royal Society of London B 269:1383–1388. It is analogous to the epidemiological “force of infection” in mathematical models for the spread of infectious diseases.

Page 130: The evidence regarding the nest-site scouts’ rule that a “discoverer-should-dance” is reported in Seeley, T D., and P. K. Visscher. 2008. Sensory coding of nest-site value in honeybee swarms. Journal of Experimental Biology 211:3691–3697.

Page 131: Several studies have carefully examined whether worker honeybees are genetically endowed with innate preferences, especially regarding the stimuli representing fowers. For reviews of classic studies on the innate search images guiding the first foraging flights of bees, see Menzel, R. 1985. Learning in honey bees in an ecological and behavioral context, in Hölldobler, B., and M. Lindauer, eds. Experimental Behavioral Ecology and Sociobiology. Gustav Fischer Verlag, Stuttgart. Pp. 55–74; and Gould, J. L., and W. F. Towne. 1987. Honey bee learning. Advances in Insect Physiology 20:55–75. For more recent original studies, see Giurfa, M., J. A. Núñ ez, L. Chittka, and R. Menzel. 1995. Colour preferences of flower-naive honeybees. Journal of Comparative Physiology A 177:247–259; Rodriguez, I., A. Gumbert, N. Hempel de Ibarra, J. Kunze, and M. Giurfa. 2004. Symmetry is in the eye of the “beholder”: innate preference for bilateral symmetry in flower-naive bumblebees. Naturwissenschaften 91:374–377.

Pages 134–135: For the full report of the study that found that neutral scouts evidently follow dances at random as they get converted into supporters, see Visscher, P. K., and S. Camazine. 1999. Collective decisions and cognition in bees. Nature 397:400. See also Camazine, S., P. K. Visscher, J. Finley, and R. S. Vetter. 1999. House-hunting by honey bee swarms: collective decision and individual behaviors. Insectes Sociaux 46:348–360.

Page 135: Mary R. Myerscough, a mathematical biologist at the University of Sydney, Australia, has created a Leslie matrix model of the population dynamics of scout bees performing dances for different nest sites. She has proven, quite elegantly, that given enough time, the dancing scouts in a swarm will almost always become focused on the one best site that has been found. See Myerscough, M. R. 2003. Dancing for a decision: a matrix model for nest-site choice by honey bees. Proceedings of the Royal Society of London B 270:577–582.

Page 136: Quote of Martin Lindauer regarding how scout bees lose interest in a lesser nest site, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 296. Translated by P. K. Visscher. Lindauer repeated in later reports his view that scouts cease advertising poorer sites after being recruited to a new and superior site and comparing the new and old sites. For example, in 1957 he wrote, “When, furthermore, those scout bees which at first had announced the inferior nesting places are won over by the more lively dances of their competitors and as a result themselves inspect this home—so that they can compare the two—then they naturally choose the better one. Hence nothing more stands in the way of an agreement.” See Lindauer, M. 1957. Communication in swarm-bees searching for a new home. Nature179:63–66. P. 64.

Page 136: Quote of Martin Lindauer regarding nest-site scouts not being stubborn, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 312. Translated by P. K. Visscher. Quote of Martin Lindauer about scouts letting their minds be changed, from Lindauer, M. 1961. Communication among Social Bees. Harvard University Press, Cambridge, MA. P. 49.

Page 137: Quote of Martin Lindauer regarding scout bees that ceased to dance for one site before they had inspected another housing possibility, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 296. Translated by P. K. Visscher.

Page 137: For a detailed discussion of the power of figuring things out by testing the predictions of competing hypotheses, see Platt, J. R. 1964. Strong inference. Science 146:347–353.

Pages 137–144: For the detailed report of the test between the compare-and-convert vs. the retire-and-rest hypotheses, see Seeley, T D. 2003. Consensus building during nest-site selection in honey bee swarms: the expiration of dissent. Behavioral Ecology and Sociobiology 53:417–424.

Page 145: Quote of Max Planck on the importance of turnover of scientists for the development of science, from Planck, M. 1950. Scientific Autobiography and Other Papers. Translated by F. Gaynor. Williams and Norgate, London. P. 33.

Page 145: For a thorough discussion of how new theories get accepted within a scientific community (i.e., how scientists make group decisions about new ideas), see Hull, D. L. 1988. Science as a Process. University of Chicago Press, Chicago.

Chapter 7. Initiating the Move to New Home

Page 146: Quote of Charles Butler, from Butler, C. 1609. The Feminine Monarchie: Or, A Treatise concerning Bees and the Divine Ordering of Them. Chapter 5, p. 14. Joseph Barnes, Oxford.

Pages 148–151: For the detailed report on Bernd Heinrich’s study of temperature regulation in honeybee swarms, see Heinrich, B. 1981. The mechanisms and energetics of honeybee swarm temperature regulation. Journal of Experimental Biology 91:25–55. He has also written a broad review of thermoregulation in insects in general. See Heinrich, B. 1993. The Hot-Blooded Insects. Harvard University Press, Cambridge, MA.

Page 150: For a detailed look at how the mantle (outermost) workers in a bivouacked swarm of honeybees adjust their body orientation, wing spread, and interindividual spacing to reduce convective heat loss from the swarm cluster, see Cully, S. M., and T. D. Seeley 2004. Self-assemblage formation in a social insect: the protective curtain of a honey bee swarm. Insectes Sociaux 51:317–324.

Pages 152–154: For the detailed report on the thermographic study of swarms warming up in preparation for flight, see Seeley, T. D., M. Kleinhenz, B. Bujok, and J. Tautz. 2003. Thorough warm-up before take-off in honey bee swarms. Naturwissenschaften 90:256–260.

Page 155: Quote of Martin Lindauer regarding which bees in a swarm produce the high-pitched piping sounds, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263-324. P. 317. Translated by P. K. Visscher.

Pages 156–162: For the detailed report of the study of scout bees producing the piping signal, see Seeley, T D., and J. Tautz. 2001. Worker piping in honey bee swarms and its role in preparing for liftoff. Journal of Comparative Physiology A 187:667–676.

Page 160: For more information on the role of the shaking or vibration signal in honeybee swarms, see Schneider, S. S., P. K. Visscher, and S. Camazine. 1998. Vibration signal behavior of waggle-dancers in swarms of the honey bee, Apis mellifera (Hymenoptera: Apidae). Ethology 104:963–972; Lewis, L. A., and S. S. Schneider. 2000. The modulation of worker behavior by the vibration signal during house hunting in swarms of the honeybee, Apis mellifera. Behavioral Ecology and Sociobiology 48:154–164; Donahoe, K., L. A. Lewis, and S. S. Schneider. 2003. The role of the vibration signal in the house-hunting process of honey bee (Apis mellifera) swarms. Behavioral Ecology and Sociobiology 54:593–600; and Pierce, A. L., L. A. Lewis, and S. S. Schneider. 2007. The use of the vibration signal and worker piping to influence queen behavior during swarming in honey bees, Apis mellifera. Ethology 113:267-275.

Pages 163–165: For the detailed report on the form and function of the buzz-run, see Rittschof, C. C, and T D. Seeley. 2008. The buzz-run: how honeybees signal “Time to go!” Animal Behaviour 75:189–197.

Page 165: The classic paper on the origins and evolution of communication signals, through the process of ritualization, is Tinbergen, N. 1952. “Derived” activities: their causation, biological significance, origin, and emancipation during evolution. Quarterly Review of Biology 27:1–32. An up-to-date treatment of signal evolution is Bradbury, J. W., and S. L. Vehrencamp. 1998. Principles of Animal Communication. Sinauer, Sunderland, MA.

Pages 166–167: Another possible example of a control system in a large social insect colony that is based on a small subset of individuals collecting information about colony state and then, when the time is right, signaling when to take action has been reported for the display tournaments between competing colonies of the honeypot ant, Myrmecocystus mimicus. See Lumsden, C. J., and B. Hölldobler. 1983. Ritualized combat and intercolony communication in ants. Journal of Theoretical Biology 100:81–98.

Pages 168–172: For detailed reports on the collaborative studies conducted by Kirk Visscher and me, to test for consensus sensing or quorum sensing, see Seeley, T. D., and P. K. Visscher. 2003. Choosing a home: how the scouts in a honey bee swarm perceive the completion of their group decision making. Behavioral Ecology and Sociobiology 54:511–520; and Seeley, T. D., and P. K. Visscher. 2004. Quorum sensing during nest-site selection by honeybee swarms. Behavioral Ecology and Sociobiology 56:594–601.

Page 171: For the detailed report on which bees produce the piping signal (only scout bees and only ones from the site where a quorum of scouts has formed), see Visscher, P. K., and T. D. Seeley. 2007. Coordinating a group departure: who produces the piping signals on honeybee swarms? Behavioral Ecology and Sociobiology 61:1615–1621.

Pages 173–174: Decision makers often face the problem of finding a suitable compromise between speedy decisions and accurate ones. The trade-off between speed and accuracy arises because if an animal has to make a fast decision then it may be prone to make a poor decision, either because it cannot sample its options sufficiently broadly or because it cannot deliberate on its options sufficiently deeply. For a recent review of this topic, see Chittka, L., P. Skorupski, and N. E. Raine. 2009. Speed-accuracy trade-offs in animal decision making. Trends in Ecology and Evolution24:400–407. For a specific study with humans, see Osman, A., L. G. Lou, H. Muller-Gethman, G. Rinkenauer, S. Mattes, and R. Ulrich. 2000. Mechanisms of speed-accuracy trade-off: evidence from covert motor processes. Biological Psychology 51:173–199. For one with bees, see Chittka, L., A. G. Dyer, F. Bock, and A. Dornhaus. 2003. Bees trade-off foraging speed for accuracy. Nature 424:388. This trade-off has also been demonstrated in ant colonies. See Franks, N. R., A. Dornhaus, J. P. Fitzsimmons, and M. Stevens. 2003. Speed versus accuracy in collective decision making. Proceedings of the Royal Society of London B 270:2457–2463.

Page 174: The Quaker method of making group decisions by consensus is described in Pollard, F. E., B. E. Pollard, and R.S.W. Pollard. 1949. Democracy and the Quaker Method. Bannisdale Press, London.

Chapter 8. Steering the Flying Swarm

Page 175: Quote of Thomas Smibert, from “The Wild Earth-Bee,” in Smibert, T 1851. Io Anche! Poems, Chiefly Lyrical. James Hogg, Edinburgh.

Page 175: The mechanisms used by honeybees to navigate to distant flowers and then find their way home are reviewed in Collett, T. S., and M. Collett. 2002. Memory use in insect visual navigation. Nature Reviews Neuroscience 3:542–552; Dyer, F. C. 1998. Spatial cognition: lessons from central-place foraging insects, in Balda, R. P., I. M. Pepperberg, and A. C. Kamil, eds. Animal Cognition in Nature. Academic Press, New York, Pp. 119–154; Menzel, R., and M. Giurfa. 2006. Dimensions of cognition in an insect, the honeybee. Behavioral and Cognitive Neuroscience Reviews5:24–40; and Wehner, R. 1992. Arthropods, in Papi, F., ed. Animal Homing. Chapman and Hall, London. Pp. 45–144.

Pages 176–177: For the detailed report of the study that demonstrated that worker bees in a flying swarm sense the presence of the queen by smelling the 9-ODA that she produces, see Avitabile, A., R. A. Morse, and R. Boch. 1975. Swarming honey bees guided by pheromones. Annals of the Entomological Society of America 68:1079-1082.

Pages 177–179: The full description of the flight of the swarm across Appledore Island in 1979 is found in Seeley, T D., R. A. Morse, and P. K. Visscher. 1979. The natural history of the flight of honey bee swarms. Psyche 86:103–113.

Pages 179–182: For the detailed report on the behaviors of the flying swarms that were tracked for 270 meters at the Liddell Field Station, see Beekman, M., R. L. Fathke, and T. D. Seeley. 2006. How does an informed minority of scouts guide a honey bee swarm as it flies to its new home? Animal Behaviour 71:161–171. This paper also reports the high flight speeds of other swarms that were tracked as they made flights of 1,000 and 4,000 meters.

Page 182: Honeybee swarms are not unique in being guided toward a target by a small fraction of the group’s members who are informed about the target’s location. For experimental studies demonstrating this in fish schools and human groups, see Reebs, S. G. 2000. Can a minority of informed leaders determine the foraging movements of a fish shoal? Animal Behaviour 59:403–409; Ward, A.J.W., D.J.T. Sumpter, I. D. Couzin, P.J.B. Hart, and J. Krause. 2008. Quorum decision making facilitates information transfer in fish shoals. Proceedings of the National Academy of Sciences, U.S.A. 105:6948-6953; and Dyer, J.R.G., C. C. Ioannou, L. J. Morrell, D. P. Croft, I. D. Couzin, D. A. Waters, and J. Krause. 2008. Consensus decision making in human crowds. Animal Behaviour 75:461–470.

Pages 182–183: The hypothesis that scouts guide the flight of a swarm with pheromones was proposed in Avitabile, A., R. A. Morse, and R. Boch. 1975. Swarming honey bees guided by pheromones. Annals of the Entomological Society of America 68:1079–1082.

Page 183: For the detailed description of the subtle guide hypothesis, and the results of computer simulations of animal groups making moves using this mechanism of guidance, see Couzin, I. D., J. Krause, N. R. Franks, and S. A. Levin. 2007. Effective leadership and decision making in animal groups on the move. Nature 433:513–516.

Page 184: Quote of Martin Lindauer regarding guiding bees flying rapidly through a swarm cloud, from Lindauer, M. 1955. Schwarmbienen auf Wohnungssuche. Zeitschrift für vergleichende Physiologie 37:263–324. P. 319. Translated by P. K. Visscher.

Page 184: For the full report of the simulation study of the streaker bee hypothesis, see Janson, S., M. Middendorf, and M. Beekman. 2005. Honeybee swarms: how do scouts guide a swarm of uninformed bees? Animal Behaviour 70:349–358.

Pages 184–187: For the full report of the study that tested the hypothesis that scout bees steer a flying swarm using the attraction pheromones produced in their scent organs, see Beekman, M., R. L. Fathke, and T. D. Seeley. 2006. How does an informed minority of scouts guide a honey bee swarm as it flies to its new home? Animal Behaviour 71:161–171.

Page 185: For a beautiful description of the anatomy of the scent organ and a review of the chemical composition of the Nasonov gland secretion, see chapter 8, Glands: chemical communication and wax production, in Goodman, L. J. 2003. Form and Function in the Honey Bee. International Bee Research Association, Cardiff.

Page 187: For the full report of the check for streaker bees using still photography, see Beekman, M., R. L. Fathke, and T. D. Seeley. 2006. How does an informed minority of scouts guide a honey bee swarm as it flies to its new home? Animal Behaviour 71:161–171.

Page 189: Quote of Kevin Passino on cooperative control strategies, from Passino, K. M. 2005. Biomimicry for Optimization, Control, and Automation. Springer Verlag, London. P. 80.

Pages 190–193: For the full report of the study in which individual bees in flying swarms were tracked using video analysis, see Schultz, K. M., K. M. Passino, and T D. Seeley. 2008. The mechanism of flight guidance in honeybee swarms: subtle guides or streaker bees? Journal of Experimental Biology 211:3287-3295.

Pages 193–195: For the full report of the experimental test of the streaker bee hypothesis, see Latty, T, M. Duncan, and M. Beekman. 2009. High bee traffic disrupts transfer of directional information in flying honeybee swarms. Animal Behaviour 78:117–121.

Chapter 9. Swarm as Cognitive Entity

Page 198: Quote of William Newsome, from the introduction to his talk delivered at the Systems Biology of Decision Making workshop, Mathematical Biosciences Institute, Ohio State University, June 17, 2008.

Page 199: The view that honeybee and other social insect colonies are elegant information-processing devices, and that there are parallels between decision making in social insect colonies and primate brains, has been developed recently in Passino, K. M., T D. Seeley, and P. K. Visscher. 2008. Swarm cognition in honey bees. Behavioral Ecology and Sociobiology 62:401–414; Couzin, I. D. 2008. Collective cognition in animal groups. Trends in Cognitive Sciences 13:36–42; and Marshall, J.A.R., R. Bogacz, A. Dornhaus, R. Planqué, T Kovacs, and N. R. Franks. 2009. On optimal decision making in brains and social insect colonies. Journal of the Royal Society Interface 6:1065-1074.

Pages 199–203: For detailed reviews of the neural basis of primate decision making, see Schall, J. D. 2001. Neural basis of deciding, choosing, and acting. Nature Reviews Neuroscience 2:33–42; Glimcher, P. W. 2003. The neurobiology of visual-saccadic decision making. Annual Review of Neuroscience 26:133-179; Glimcher, P. W. 2003. Decisions, Uncertainty and the Brain: The Science of Neuroeconomics. MIT Press, Cambridge, MA; Gold, J. I., and M. N. Shadlen. 2007. The neural basis of decision making. Annual Review of Neuroscience 30:535–574; and Heekeren, H. R., S. Marrett, and L. G. Ungerleider. 2008. The neural systems that mediate human perceptual decision making. Nature Reviews Neuroscience 9:467–479.

Pages 203-204: The Sugrue-Corrado-Newsome framework for thinking about the stages of information processing in making decisions is presented in Sugrue, L. P., G. S. Corrado, and W. T Newsome. 2005. Choosing the greater of two goods: neural currencies for valuation and decision making. Nature Reviews Neuroscience 6:363–375.

Page 210: The Usher-McClelland model of decision making in the primate visual cortex is described in Usher, M., and J. L. McClelland. 2001. The time course of perceptual choice: the leaky, competing accumulator model. Psychological Review 108:550–592. An earlier connectionist model of decision making, which is likewise based on the idea that information is sequentially sampled and accumulated over time to make a decision, is described in Busmeyer, J. R., and J. T Townsend. 1993. Decision field theory: a dynamic cognition approach to decision making. Psychological Review 100:432–459. For an excellent general review of the decision models that have been developed by mathematical psychologists, see Smith, P. L., and R. Ratcliff. 2004. Psychology and neurobiology of simple decisions. Trends in Neurosciences 27:161–168.

Pages 210–213: For the full report of the mathematical modeling of the nest-site selection by honeybee swarms, which includes the analysis of how the dance decay rate and the quorum size have been tuned by natural selection to achieve a good balance between speed and accuracy in a swarm’s decision making, see Passino, K. M., and T. D. Seeley. 2006. Modeling and analysis of nest-site selection by honeybee swarms: the speed and accuracy trade-of. Behavioral Ecology and Sociobiology 59:427-442.

Page 213: See Hofstadter, D. R. 1979. Gödel, Escher, Bach:An Eternal Golden Braid. Basic Books, New York.

Page 215: For overviews of the analysis of collective nest choice by colonies of rock ants, see Mallon, E. B., S. C. Pratt, and N. R. Franks. 2001. Individual and collective decision making during nest site selection by the ant Leptothorax albipennis. Behavioral Ecology and Sociobiology50:352–359; Franks, N. R., S. C. Pratt, E. B. Mallon, N. F. Britton, and D.J.T. Sumpter. 2002. Information flow, opinion polling and collective intelligence in house- hunting social insects. Philosophical Transactions of the Royal Society of London B 357:1567–1583; Pratt, S. C, D. J.T. Sumpter, E. B. Mallon, and N. R. Franks. 2005. An agent-based model of collective nest choice by the ant Temnothorax albipennis. Animal Behaviour 70:1023–1036; and Franks, N. R., F.-X. Dechaume-Moncharmont, E. Hanmore, and J. K. Reynolds. 2009. Speed versus accuracy in decision-making ants: expediting politics and policy implementation. Philosophical Transactions of the Royal Society B 364:845–852.

Pages 215–217: For the full analysis of how social insect colonies may be able to achieve statistically optimal collective decision making in a way similar to primate brains via competition between populations of evidence-accumulating subunits (workers or neurons), see Marshall, J.A.R., R. Bogacz, A. Dornhaus, R. Planqué, T. Kovacs, and N. R. Franks. 2009. On optimal decision making in brains and social insect colonies. Journal of the Royal Society Interface 6:1065–1074. This paper rests on a foundation of theoretical studies of optimal decision making. See, for example, Bogacz, R., E. Brown, J. Moehlis, P. Holmes, and J. D. Cohen. 2006. The physics of optimal decision making: a formal analysis of models of performance in two-alternative force choice tasks. Psychological Review 113:700–765.

Chapter 10. Swarm Smarts

Page 218: Quote of William Shakespeare, from Shakespeare, W. 1599. Henry V. Act I, scene 2, lines 190–192.

Page 218: For general discussions of how a group of humans working face to face can be organized so that the many are reliably smarter than the few, see Elster, J. 2000. Deliberative Democracy. Cambridge University Press, Cambridge; Surowiecki, J. 2004. The Wisdom of Crowds.Doubleday, New York; and Austen-Smith, D., and T. J. Feddersen. 2009. Information aggregation and communication in committees. Philosophical Transactions of the Royal Society B 364:763–769.

Page 218: For authoritative reviews on the fossil record of honeybees (genus Apis), see Engel, M. S. 1998. Fossil honey bees and evolution in the genus Apis (Hymenoptera: Apidae). Apidologie 29:265–281; Engel, M. S. 1999. The taxonomy of recent and fossil honey bees (Hymenoptera: Apidae: Apis). Journal of Hymenoptera Research 8:165–196; Engel, M. S. 2006. A giant honey bee from the middle Miocene of Japan (Hymenoptera: Apidae). Journal of the Kansas Entomological Society 76:71; and Engel, M. S., I. A. Hinojosa-Diaz, and A. Rasnitsyn. 2009. A honey bee from the Miocene of Nevada and the biogeography of Apis (Hymenoptera: Apidae: Apini). Proceedings of the California Academy of Sciences 60:23–38.

Page 219: The expression “The Five Habits of Highly Effective Groups” is inspired by the title of Stephen R. Covey’s excellent book, The Seven Habits of Highly Effective People. 1989. Free Press, New York.

Page 219: The New England town meeting is a law-making legislative assembly in which every participating citizen (registered voter) is a legislator. It should not be confused with the “town hall meeting” that has become a popular form of public hearing but is not an assembly that has the force of law. For information on how the New England town meeting works, see Gould, J. 1940. New England Town Meeting: Safeguard of Democracy. Stephen Daye Press, Brattleboro, VT; Mansbridge, J. J. 1980. Beyond Adversary Democracy. University of Chicago Press, Chicago; and Bryan, F. M. 2004. Real Democracy:The New England Town Meeting and How It Work. University of Chicago Press, Chicago.

Page 222: The importance of avoiding leadership practices that bias the group’s decision making and foster concurrence-seeking is discussed in detail in Janis, I. L. 1982. Groupthink. 2nd ed. Houghton Miffin, Boston.

Page 223: For a description of the leadership style of President George W. Bush (instinctive rather than intellectual) and how he and his foreign policy team decided to invade Iraq without undertaking an open inquiry and critical evaluation of all possible options, see Mc-Clellan, S. 2008. What Happened. Public Affairs, New York. Pp. 126–129.

Page 223: For the latest version of the rules of parliamentary law first published in 1876 by Major Henry M. Robert, see Robert, H. M., and S. C. Robert. 2000. Robert’s Rules of Order Newly Revised, 10th Edition. Perseus Publishing, Philadelphia.

Page 224: For a broad review of how a group of individuals can find better solutions to problems than can a brilliant individual working alone, based in large measure on the group’s superior ability to explore diverse options, see Page, S. E. 2007. The Difference. Princeton University Press, Princeton, NJ.

Page 226: For an overview of human voting systems and a discussion of the merits of various decision procedures, see Black, D. 1986. The Theory of Committees and Elections. Kluwer, Dordrecht.

Page 226: For reviews of the literature on democratic decision making in groups of non-human animals, see Conradt, L., and T. J. Roper. 2003. Group decision making in animals. Nature 421:155–158; Conradt, L., and T. J. Roper. 2005. Consensus decision making in animals. Trends in Ecology and Evolution 20:449–456; Conradt, L. and T. J. Roper. 2007. Democracy in animals: the evolution of shared group decisions. Proceedings of the Royal Society of London B 274:2317–2326; Conradt, L., and C. List. 2009. Introduction. Group decisions in humans and animals: a survey. Philosophical Transactions of the Royal Society B 364:719–742.

Pages 226–228: A recent modeling study shows explicitly how the bees’ collective decision-making system depends on both interdependence and independence among the scout bees. Without interdependence (by sharing information about sites with dances), there is no cascading of interest on the best site. Without independence (in assessing and then advertising sites), there is a cascading of interest but not necessarily on the best site. For details, see List, C, C. Elsholtz, and T. D. Seeley. 2009. Independence and interdependence in collective decision making: an agent-based model of nest-site choice by honeybee swarms. Philosophical Transactions of the Royal Society B 364:755-762.

Page 228: For more examples of the danger of information cascades, when decision makers blindly copy the decisions others, see Shiller, R. J. 2000. Irrational Exuberance. Princeton University Press, Princeton, NJ; and Thaler, R. H., and C. R. Sunstein. 2008. Nudge. Yale University Press, New Haven, CT. Two important articles on the topic are Bikhchandani, S., D. Hirshleifer, and I. Welch. 1992. A theory of fads, fashions, custom, and cultural change as informational cascades. Journal of Political Economy 100:992–1026; and Bikhchandani, S., D. Hirshleifer, and I. Welch. 1998. Learning from the behavior of others: conformity, fads, and informational cascades. Journal of Economic Perspectives 12:151–170.

Pages 230–231: For a general discussion of the utility of quorum responses in building consensus decisions (i.e., when group members come to agree on the same option), see Sumpter, D.J.T., and S. C. Pratt. 2009. Quorum responses and consensus decision making. Philosophical Transactions of the Royal Society B 364:743-753.

Epilogue

Page 233: Quote of Martin Lindauer regarding beautiful experience, from Seeley, T. D., S. Kühnholz, and R. H. Seeley. 2002. An early chapter in behavioral physiology and sociobiology: the science of Martin Lindauer. Journal of Comparative Physiology A 188:439–45 3. P. 447.

Page 233: Unfortunately, it is difficult to apply the honeybees’ lessons about good democratic decision making to groups composed of individuals with strongly conflicting interests. In such adversarial groups, individuals will not behave like scout bees: totally honest and reliably hardworking. They are instead expected to issue lies and act lazily when doing so provides them with benefits even if doing so degrades the group’s success. Nevertheless, because many small democratic organizations are composed of people with strongly overlapping interests, I feel the lessons learned from the house-hunting bees have considerable relevance to human affairs.