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3 - Schooling by continuously active fishes: Clues to sleep's ultimate function

Published online by Cambridge University Press:  10 March 2010

By
J. Lee Kavanau
Edited by
Patrick McNamara ,
Robert A. Barton  and
Charles L. Nunn
Patrick McNamara
Affiliation:
Boston University
Robert A. Barton
Affiliation:
University of Durham
Charles L. Nunn
Affiliation:
Max Planck Institute for Evolutionary Anthropology
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Summary

Introduction

Aquatic habitats were the cradle of sleep many million years before sleep evolved in terrestrial animals. Yet these habitats were the last to be explored in seeking sleep's ultimate function, which I have suggested to be the enabling of highly efficient brain operation at all times. Although the sleep of most fishes is essentially indistinguishable from that of terrestrial vertebrates, by exploiting the rich variety and greater permissiveness of aquatic habitats, some fishes have bypassed a need for sleep. In three continuously active states, they purportedly achieve comparable, and even greater, benefits than is provided by sleep, yet remain perpetually vigilant.

I propose that “schooling” (swimming synchronously in polarized groups) by these fishes plays a major role in the lack of a need for sleep. Thus, by schooling, they are able to achieve sleep's benefits without closing or occluding their eyes, namely, a great reduction in the average school member's reception and processing of external sensory input. Because the evident benefits of schooling by some fishes substitute for the obscure benefits of sleep by closely related fishes, the evident benefits give clues to the obscure ones. These clues support views on the ultimate function of sleep.

After reviewing circumstances relating to the evolution of sleep in terrestrial animals, relevant topics in the lives of fishes are treated, emphasizing their sleep and its awake, almost equivalent functions with eyes open.

Type
Chapter
Information
Evolution of Sleep
Phylogenetic and Functional Perspectives
 , pp. 57 - 85
Publisher: Cambridge University Press
Print publication year: 2009

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References

Beamish, F. H. A. (1978). Swimming capacity. In Hoar, W. S. & Randall, D. J. (Eds.), Fish physiology (Vol. 7, pp. 101–187). London: Academic Press.Google Scholar
Blaxter, J. H. S. (1965). Effect of change of light intensity on fish. International Commission Northwest Atlantic Fisheries Special Publications, 6, 647–661.Google Scholar
Blaxter, J. H. S. (1988). Sensory performance, behavior, and ecology of fish. In Atema, J., Fay, R. R., Popper, A. N., & Tavolga, W. N. (Eds.), Sensory biology of aquatic animals (pp. 203–232). New York: Springer-Verlag.CrossRefGoogle Scholar
Bleckmann, H. (1993). Role of the lateral line in fish behaviour. In Pitcher, T. J. (Ed.), Behaviour of teleost fishes (pp. 201–246). London: Chapman & Hall.CrossRefGoogle Scholar
Block, B. A. (1991). Endothermy in fish: Thermogenesis, ecology, and evolution. In Hochachka, P. W. & Mommsen, T. P. (Eds.), Biochemistry and molecular biology of fishes (Vol. 1, pp. 269–311). Oxford: Elsevier.Google Scholar
Bowen, E. S. (1931). The role of the sense organs in aggregations of Ameiurus melas. Ecological Monographs, 1, 1–35.CrossRefGoogle Scholar
Breder, C. M. (1967). On the survival of fish schools. Zoologica, 52, 25–40.Google Scholar
Breder, C. M. (1976). Fish schools as operational structures. Fisheries Bulletin, 47, 471–502.Google Scholar
Brock, V. E. (1965). A review of the effects of the environment on the tuna. International Commission Northwest Atlantic Fisheries Special Publications, 6, 75–92.Google Scholar
Buzsáki, G. (2006). Rhythms of the brain. New York: Oxford University Press.CrossRefGoogle Scholar
Collette, B. B. (1977). Adaptations and systematics of the mackerels and tunas. In Sharp, G. D. & Dizon, A. E. (Eds.), The physiological ecology of tunas (pp. 7–39). New York: Academic Press.Google Scholar
Collette, B. B., & Nauen, C. E. (1983). Scombrids of the world. Rome: FAO Fisheries Synopsis, 125(2), 1–137.Google Scholar
Cousteau, J. Y., & Cousteau, P. (1970). The shark: Splendid savage of the sea. New York: Doubleday & Co, Inc.Google Scholar
Cushing, D. H., & Jones, F. R. H. (1968). Why do fish school?Nature, 218, 918–920.CrossRefGoogle ScholarPubMed
Denton, E. J., & Gray, J. A. B. (1988). Mechanical factors in the excitation of the lateral lines of fishes. In Atema, J., Fay, R. R., Popper, A. N., & Tavolga, W. N. (Eds.), Sensory biology of aquatic animals (pp. 596–617). New York: Springer-Verlag.Google Scholar
Dizon, A. E., Brill, R. W., & Yuen, H. S. H. (1977). Correlations between environment, physiology, and activity and the effects on thermoregulation in skipjack tuna. In Sharp, G. D. & Dizon, A. E. (Eds.), The physiological ecology of tunas (pp. 233–239). New York: Academic Press.Google Scholar
Douglas, R. H., & Hawryshyn, C. W. (1990). Behavioural studies of fish vision: An analysis of visual capabilities. In Douglas, R. & Djamgoz, M. (Eds.), The visual system of fish (pp. 373–418). London: Chapman & Hall.CrossRefGoogle Scholar
Fernald, R. D. (1988). Aquatic adaptations in fish eyes. In Atema, J., Fay, R. R., Popper, A. N., & Tavolga, W. N. (Eds.), Sensory biology of aquatic animals (pp. 435–466). Berlin: Springer-Verlag.CrossRefGoogle Scholar
Fernald, R. D. (1991). Teleost vision: Seeing while growing. Journal of Experimental Zoology, 5(Suppl.), 167–180.Google Scholar
Fernald, R. D. (1993). Vision. In Evans, D. H. (Ed.), The physiology of fishes (pp. 161–189). London: CRC Press.Google Scholar
Gerking, S. D. (1994). Feeding ecology of fish. New York: Academic Press.Google Scholar
Gibson, R. N. (1993). Intertidal teleosts: Life in a fluctuating environment. In Pitcher, T. J. (Ed.), The behaviour of teleost fishes (pp. 513–536). London: Chapman & Hall.CrossRefGoogle Scholar
Goldshmid, G., Holzman, R., Weihs, D., & Genin, A. (2004). Aeration of corals by sleep-swimming fish. Limnology Oceanography, 49, 1832–1839.CrossRefGoogle Scholar
Grunbaum, D. (1997). Schooling as a strategy for taxis in a noisy environment. In Parrish, J. K. & Hamner, W. M. (Eds.), Animal groups in three dimensions (pp. 257–281). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Guthrie, D. M. (1981). Visual central processes in fish behavior. In Ewert, J. P., Capranica, R. R., & Ingle, D. J. (Eds.), Advances in vertebrate neuroethology (pp. 381–412). London: Plenum Press.Google Scholar
Guthrie, D. M. (1986). Role of vision in fish behavior. In Pitcher, T. J. (Ed.), The behavior of teleost fishes (pp. 75–113). Baltimore: Johns Hopkins University Press.CrossRefGoogle Scholar
Guthrie, D. M. (1990). The physiology of the teleostean optic tectum. In Douglas, R. & Djamgoz, M. (Eds.), The visual system of fish (pp. 279–343). London: Chapman & Hall.CrossRefGoogle Scholar
Hamner, W. M. (1984). Aspects of schooling in Euphausia superba. Journal of Crustacean Biology, 4(Spec. No. 1), 67–74.CrossRefGoogle Scholar
Hamner, W. M. (1995). Predation, cover, and convergent evolution in epipelagic oceans. Marine and Freshwater Behaviour and Physiology, 26, 71–89.CrossRefGoogle Scholar
Hart, P. J. B. (1993). Teleost foraging: Facts and theories. In Pitcher, T. J. (Ed.), The behaviour of teleost fishes (pp. 254–284). London: Chapman & Hall.Google Scholar
Hawkins, A. D. (1993). Underwater sound and fish behaviour. In Pitcher, T. J. (Ed.), The behaviour of teleost fishes (pp. 129–169). London: Chapman & Hall.CrossRefGoogle Scholar
Hazel, J. R. (1993). Thermal biology. In Evans, D. H. (Ed.), The physiology of fishes (pp. 427–467). London: CRC Press.Google Scholar
Helfman, G. S. (1986). Behavioral responses of prey fishes during predator-prey interactions. In Feder, M. E. & Lauder, G. V. (Eds.), Predator-prey relationships (pp. 135–156). Chicago: University of Chicago Press.Google Scholar
Helfman, G. S. (1993). Fish behavior by day, night, and twilight. In Pitcher, T. J. (Ed.), The behaviour of teleost fishes (pp. 479–512). London: Chapman & Hall.CrossRefGoogle Scholar
Herald, E. S. (1961). Living fishes of the world. New York: Doubleday & Co.Google Scholar
Hobson, E. S. (1972). Activity of Hawaiian reef fishes during the evening and morning transitions between daylight and darkness. Fisheries Bulletin of the National Marine Fisheries Service, 70, 715–740.Google Scholar
Hobson, E. S. (1974). Feeding relationships of teleostean fishes on coral reefs in Kona, Hawaii. Fisheries Bulletin of the National Marine Fisheries Service, 72, 915–1031.Google Scholar
Huntingford, F. A. (1993). Development of behavior in fish. In Pitcher, T. J. (Ed.), The behaviour of teleost fishes (pp. 59–83). London: Chapman & Hall.Google Scholar
Imamura, Y. (1951). The Japanese skipjack fishery (W. G. Van Campen, trans.). Washington, D.C.: U. S. Fish and Wildlife Service Special Scientific Report, Fisheries, 49, 1–67.Google Scholar
Janvier, P. (1996). Early vertebrates. Oxford: Clarendon Press.Google Scholar
Jobling, M. (1993). Bioenergetics: Feed intake and energy partitioning. In Rankin, J. C. & Jensen, F. B. (Eds.), Fish ecophysiology (pp. 1–44). London: Chapman & Hall.Google Scholar
John, K. R. (1964). Illumination, vision, and schooling of Astyanax mexicanus (Fillipi). Journal of the Fisheries Research Board of Canada, 23, 547–562.Google Scholar
Kavanau, J. L. (1997a). Memory, sleep, and the evolution of mechanisms of synaptic efficacy maintenance. Neuroscience, 79, 7–44.CrossRefGoogle ScholarPubMed
Kavanau, J. L. (1997b). Origin and evolution of sleep: Roles of vision and endothermy. Brain Research Bulletin, 42, 245–264.CrossRefGoogle ScholarPubMed
Kavanau, J. L. (1998). Vertebrates that never sleep: Implications for sleep's basic function. Brain Research Bulletin, 46, 269–279.CrossRefGoogle ScholarPubMed
Kavanau, J. K. (2005). Evolutionary approaches to understanding sleep. Sleep Medicine Reviews, 9, 141–152.CrossRefGoogle Scholar
Keenleyside, M. H. A. (1979). Diversity and adaptation in fish behaviour. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Kitchell, J. F., Neill, W. H., Dizon, A. E., & Magnusen, J. J. (1977). Bioenergetic spectra of skipjack and yellowfin tunas. In Sharp, G. D. & Dizon, A. E. (Eds.), The physiological ecology of tunas (pp. 357–368). New York: Academic Press.Google Scholar
Levine, J. S. (1993). The coral reef at night. New York: Harry N. Abrams.Google Scholar
Llinás, R. R., & Paré, D. (1991). Of dreaming and wakefulness. Neuroscience, 44, 521–535.CrossRefGoogle ScholarPubMed
Long, J. A. (1995). The rise of fishes. Baltimore: The Johns Hopkins University Press.Google Scholar
Lowe-McConnell, R. H. (1977). Ecology of fishes in tropical waters. London: Edward Arnold.Google Scholar
Lowe-McConnell, R. H. (1987). Ecological studies in tropical fish communities. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Lythgoe, J. N. (1979). The ecology of vision. Oxford: Clarendon Press.Google Scholar
Magnuson, J. L. (1977). Foreword. In Sharp, G. D. & Dizon, A. E. (Eds.), The physiological ecology of tunas (pp. xi–xiii). New York: Academic Press.Google Scholar
Magnuson, J. L. (1978). Locomotion by scombrid fishes; hydromechanics, morphology, and behaviour. In Hoar, W. S. & Randall, D. J. (Eds.), Fish physiology (Vol. 7, pp. 239–313). New York: Academic Press.Google Scholar
Magnuson, J. L. & Weininger, D. (1977). Estimation of minimum sustained speed and associated body drag of scombrids. In Sharp, G. D. & Dizon, A. E. (Eds.), The physiological ecology of tunas (pp. 287–311). New York: Academic Press.Google Scholar
Magurran, A. E. (1993). Individual differences and alternative behaviours. In Pitcher, T. J. (Ed.), The behaviour of teleost fishes (pp. 441–477). London: Chapman & Hall.CrossRefGoogle Scholar
Maquet, P. (2001). The role of sleep in learning and memory. Science, 294, 1048–1052.CrossRefGoogle ScholarPubMed
McFarland, W. N., Ogden, J. C., & Lythgoe, J. N. (1979). The influence of light on the twilight migration of grunts. Environmental Biology of Fishes, 4, 9–22.CrossRefGoogle Scholar
McFarland, W. N., & Hillis, Z. M. (1982). Observations on agonistic behavior between members of juvenile French and white grunts. Bulletin of Marine Science, 32, 255–268.Google Scholar
Migdalski, E. C., & Fichter, G. S. (1976). The freshwater and saltwater fishes of the world. New York: A. A. Knopf.Google Scholar
Morrow, J. E.. (1948). Schooling behavior in fishes. Quarterly Review of Biology, 23, 27–38.CrossRefGoogle ScholarPubMed
Moyle, P. B., & Cech, , , J. J. (1996). The fishes: An introduction to ichthyology. Upper Saddle River, NJ: Prentice Hall.Google Scholar
Muntz, W. R. A. (1977). The visual world of the amphibia. Handbook of Sensory Physiology, VII(5), 275–307.CrossRefGoogle Scholar
Muntz, W. R. A. (1990). Stimulus, environment, and vision in fishes. In Douglas, R. H. & Djamgoz, M. B. A. (Eds.), The visual system of fish (pp. 491–511). New York: Chapman & Hall.CrossRefGoogle Scholar
Munz., F. W., & McFarland, W. N. (1977). Evolutionary adaptations of fishes to the photic environment. Handbook of Sensory Physiology, VII(5), 193–274.CrossRefGoogle Scholar
Myrberg, A. A. (1997). Underwater sound: Its relevance to behavioral functions among fishes and mammals. Marine and Freshwater Behaviour and Physiology, 29, 3–21.CrossRefGoogle Scholar
Nakamura, H. (1954). Tuna longline fishery and fishing grounds (Van Campen, W. G., trans.). Washington, D.C.: U.S. Fish and Wildlife Service Special Scientific Report, Fisheries, No. 112.
Nilsson, G. E., Hobbs, J. P. A., & Ostlund-Nilsson, S. (2007). Tribute to P. L. Lutz: Respiratory physiology of coral-reef teleosts. Journal of Experimental Biology, 210, 1673–1686.CrossRefGoogle Scholar
Noakes, D. L. G., & Godin, J. G. J. (1988). Ontogeny of behavior and concurrent developmental changes in sensory systems in teleosts. In Hoar, W. S. & Randall, D. J. (Eds.), Fish physiology, XIB (pp. 345–395). New York: Academic Press.Google Scholar
Norman, J. R. (1931). A history of fishes. New York: F. H. Stokes.Google Scholar
Norris, K. S., & Schilt, C. R. (1988). Cooperative societies in three-dimensional space: On the origin of aggregations, flocks, and schools, with special reference to dolphins and fish. Ethology and Sociobiology, 9, 146–179.CrossRefGoogle Scholar
Partridge, B. L., & Pitcher, T. J. (1980). The sensory basis of fish schools: Relative roles of lateral line and vision. Journal of Comparative Physiology, 135, 315–325.CrossRefGoogle Scholar
Pitcher, T. J., & Parrish, J. K. (1993). Functions of shoaling behavior in teleosts. In Pitcher, J. G. (Ed.), The behaviour of teleost fishes (pp. 363–439). London: Chapman & Hall.CrossRefGoogle Scholar
Popper, A. N., Rogers, P. H., Saidel, W. M., & Cox, M. (1988). Role of the fish ear in sound processing. In Atema, J., Fay, R. R., Popper, A. N., & Tavolga, W. (Eds.), Sensory biology of aquatic animals (pp. 687–710). New York: Springer-Verlag.CrossRefGoogle Scholar
Rauschecker, J. (1995). Developmental plasticity and memory. Behavioural Brain Research, 66, 7–12.CrossRefGoogle ScholarPubMed
Reebs, S. (1992). Sleep, inactivity, and circadian rhythms in fish. In Ali, M. A. (Ed.), Rhythms in fishes (pp. 127–135). New York: Plenum Press.CrossRefGoogle Scholar
Ritz, D. A. (1997). Costs and benefits as a function of group size: Experiments on a swarming mysid Paramesopodopsis rufa Fenton. In Parrish, J. K. & Hamner, W. M. (Eds.), Animal groups in three dimensions (pp. 194–224). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Rivas, L. R. (1977). Preliminary models of annual life history cycles of the North Atlantic bluefin tuna. In Sharp, G. D. & Dizon, A. E. (Eds.), The physiological ecology of tunas (pp. 369–393). New York: Academic Press.Google Scholar
Sella, M. (1952). Migrations and habitat of the tuna (Thunnus thynnus) (Van Campen, W. G., trans.). Washington, D.C.: U.S. Fish and Wildlife Service Special Scientific Report, Fisheries, 76, 1–20.Google Scholar
Sette, O. E. (1950). Biology of the Atlantic mackerel (Scomber scombrus) of North America, Part II. Migrations and habits. U.S. Fisheries & Wildlife Service Fisheries Bulletin, 51(49), 251–358.Google Scholar
Shapiro, C. M., & Hepburn, H. R. (1976). Sleep in a schooling fish, Tilapia mossambica. Physiology and Behavior, 16, 613–615.CrossRefGoogle Scholar
Sharp, G. D., & Vlymen, W. J., III. (1977). The relation between heat generation, conservation, and the swimming energetics of tuna. In Sharp, G. D. & Dizon, A. E. (Eds.), The physiological ecology of tunas (pp. 213–232). New York: Academic Press.Google Scholar
Shaw, E. (1970). Schooling in fishes: Critique and review. In Aronson, L. R., Tobach, E., Lehrman, D. S., & Rosenblatt, J. S. (Eds.), Development and evolution of behavior (pp. 452–480). San Francisco: W. H. Freeman.Google Scholar
Shaw, E. (1978). Schooling fishes. American Scientist, 66, 166–175.Google Scholar
Shimada, B. M., & Van Campen, W. G. (1951). Tuna fishing in Palau waters. Washington, D.C.: U.S. Fish and Wildlife Service Special Scientific Report, Fisheries, No. 42, 1–26.Google Scholar
Siegmund, R. Lokomotorische (1969). Aktivitat und Ruheverhalten bei einheimischen Susswasserfischen (Pisces, Percidae, Cyprinidae). Biologisches Zentralblatt, 88, 295–312.Google Scholar
Smith, M. M., & Heemstra, P. C. (1986). Smiths' sea fishes. New York: Springer-Verlag.CrossRefGoogle Scholar
Tamura, T. (1968). Fundamental studies on the visual sense in fish. In Kristjonsson, H. (Ed.), Modern fishing gear of the world (pp. 543–547). London: Fishing News (Books) Ltd.Google Scholar
Tauber, E. S., Weitzman, E. D., & Korey, S. R. (1939). Eye movements during behavioral inactivity of certain Bermuda reef fish. Communications in Behavioral Biology, 3, 131–135.Google Scholar
Tiews, K. F. W. (1963). Behavior and physiology. FAO (FAU UN) Fisheries Report, 6(1), 44–46.Google Scholar
Turner, G. (1993). Teleost mating behaviour. In Pitcher, T. J. (Ed.), The behaviour of teleost fishes (pp. 307–331). London: Chapman & Hall.CrossRefGoogle Scholar
Wagner, H. J. (1990). Retinal structure of fishes. In Douglas, R. & Djamgoz, M. (Eds.), The visual system of fish (pp. 109–157). London: Chapman & Hall.CrossRefGoogle Scholar
Warburton, K. (1997). Social forces in animal congregations: Interactive, motivational, and sensory aspects. In Parrish, J. K & Hamner, W. M. (Eds.), Animal groups in three dimensions (pp. 313–336). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Wardle, C. S. (1985). Swimming activity in marine fish. In Laverack, M. S. (Ed.), Physiological adaptations of marine animals (pp. 521–540). Scarborough: The Co. of Biologists Ltd.Google Scholar
Weber, E. (1961). Über Ruhelagen von Fischen. Zeitschrift für Tierpsychologie, 18, 517–533.Google Scholar
Welcomme, R. L. (1985). River fisheries. FAO Fisheries Technical Paper (Rome), 262, 1–330.Google Scholar
Wootton, R. J. (1992). Fish ecology. New York: Chapman & Hall.CrossRefGoogle Scholar
Yuen, H. S. H. (1962). Schooling behavior within aggregations composed of yellowfin and skipjack tuna. FAO (FAO UN) Fisheries Report, 6(3), 1419–1429.Google Scholar
Yuen, H. S. H. (1970). Behavior of skipjack tuna, Katsuwonus pelamis, as determined by tracking with ultrasonic devices. Canadian Fisheries Research Board, 27, 2071–2079.CrossRefGoogle Scholar

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