Advertisement

Environmental Biology of Fishes

, Volume 60, Issue 1–3, pp 225–250 | Cite as

Review of Elasmobranch Behavioral Studies Using Ultrasonic Telemetry with Special Reference to the Lemon Shark, Negaprion Brevirostris, Around Bimini Islands, Bahamas

  • L. Fredrik Sundström
  • Samuel H. Gruber
  • Susi M. Clermont
  • João P.S. Correia
  • Jean R.C. de Marignac
  • John F. Morrissey
  • Courtney R. Lowrance
  • Lori Thomassen
  • Miguel T. Oliveira
Article

Abstract

A review of past behavioral ultrasonic telemetry studies of sharks and rays is presented together with previously unpublished material on the behavior of the lemon shark, Negaprion brevirostris, around the Bimini Islands, Bahamas. The review, focusing on movement behaviors of 20 shark and three ray species, reveals that elasmobranchs exhibit a variety of temporal and spatial patterns in terms of rates-of-movement and vertical as well as horizontal migrations. The lack of an apparent pattern in a few species is probably attributable to the scarcity of tracking data. Movements are probably governed by several factors, some still not studied, but data show that food, water temperature, bottom type, and magnetic gradient play major roles in a shark's decision of where and when to swim. A few species exhibit differences in behavior between groups of sharks within the same geographical area. This interesting finding warrants further research to evaluate the causes of these apparent differences and whether these groups constitute different subpopulations of the same species. The lack of telemetry data on batoids and some orders of sharks must be addressed before we can gain a more comprehensive understanding of the behavior of elasmobranch fishes. Previously unpublished data from 47 smaller and 38 larger juvenile lemon sharks, collected over the decade 1988–1998, provide new results on movement patterns, habitat selection, activity rhythms, swimming speed, rate-of-movement, and homing behavior. From these results we conclude that the lemon shark is an active predator with a strong, apparently innate homing mechanism. This species shows ontogenetic differences in habitat selection and behavior, as well as differences in movements between groups of individuals within the same area. We suggest three hypotheses for future research on related topics that will help to understand the enigmatic behavior of sharks.

movement pattern swimming speed transmitter homing rate-of-movement 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ackerman, J.T., M.C. Kondratieff, S.A. Matern & J.J. Cech. 2000. Tidal influence on spatial dynamics of leopard sharks, Triakis semifasciata, in Tomales Bay, California. Env. Biol. Fish. 58: 33–43.Google Scholar
  2. Alcock, J. 1993. Animal behavior. Sinauer Associates, Sunderland. 625 pp.Google Scholar
  3. Anderson, S.D. & K.J. Goldman. 1996. Photographic evidence of white shark movements in California waters. Calif. Fish. Game 82: 182–186.Google Scholar
  4. Bass, G.A. & M. Rascovich. 1965. Adevice for the sonic tracking of large fishes. Zoologica 50: 75–83.Google Scholar
  5. Bathurst, R.G.C. 1967. Ölitic films on lowenergy carbonate sand grains, Bimini Lagoon, Bahamas. Mar. Geol. 5: 89–109.Google Scholar
  6. Becker, J.B, S.M. Breedlove & D. Crews. 1992. Behavioral endocrinology. The MIT Press, Cambridge. 574 pp.Google Scholar
  7. Blaylock, R.A. 1990. Effects of external biotelemetry transmitters on behavior of the cownose ray Rhinoptera bonasus (Mitchill 1815). J. Exp. Mar. Biol. Ecol. 141: 213–220.Google Scholar
  8. Bone, Q. 1988. Muscles and locomotion. pp. 99–141. In: T.J. Shuttleworth (ed.) Physiology of Elasmobranch Fishes, Springer-Verlag, Berlin.Google Scholar
  9. Bradbury, J.W. & S.L. Vehrencamp. 1998. Principles of animal communication. Sinauer Associates, Sunderland. 882 pp.Google Scholar
  10. Brown, C.A. & S.H. Gruber. 1988. Age assessment of the lemon shark, Negaprion brevirostris, using tetracycline validated vertebral centra.Copeia 1988: 747–753.Google Scholar
  11. Bushnell, P.G., P.L. Lutz & S.H. Gruber. 1989. The metabolic rate of an active, tropical elasmobranch, the lemon shark (Negaprion brevirostris). Exp. Biol. 48: 279–283.Google Scholar
  12. Carey, F.G. & E. Clark. 1995. Depth telemetry from the sixgill shark, Hexanchus griseus, at Bermuda. Env. Biol. Fish. 42: 7–14.Google Scholar
  13. Carey, F.G. & Q.H. Gibson. 1987. Blood flow in the muscle of free-swimming fish. Physiol. Zool. 60: 138–148.Google Scholar
  14. Carey, F.G. & B.H. Robinson. 1981. Daily patterns in the activities of swordfish, Xiphias gladius, observed by acoustic telemetry. U.S. Fish. Bull. 79: 277–292.Google Scholar
  15. Carey, F.G. & J.V. Scharold. 1990. Movements of blue sharks (Prionace glauca) in depth and course. Mar. Biol. 106: 329–342.Google Scholar
  16. Carey, F.G., J.W. Kanwisher, O. Brazier, G. Gabrielson, J.G. Casey & H.L. Pratt, Jr. 1982. Temperature and activities of a white shark, Carcharodon carcharias. Copeia 1982: 254–260.Google Scholar
  17. Carey, F.G., J.M. Teal & J.W. Kanwisher. 1981. The visceral temperatures of mackerel sharks (Lamnidae). Physiol. Zool. 54: 334–344.Google Scholar
  18. Casey, J.G. & N.E. Kohler. 1990. Long distance movements of Atlantic sharks from the NMFS cooperative shark tagging program. pp. 87–91. In: S.H. Gruber (ed.) Discovering Sharks, Underwater Naturalist, Highlands.Google Scholar
  19. Cohen, J.L. 1991. Adaptations for scotopic vision in the lemon shark. J. Exp. Zool. suppl. 5: 76–84.Google Scholar
  20. Compagno, L.J.V. 1984. FAO species catalogue of the world, vol 4: Sharks of the world. An annotated and illustrated catalogue of shark species known to date, part 2: Carcharhiniformes. FAO Fish. Synop. 125, Vol. 4, Pt.2: 251–665.Google Scholar
  21. Cortés, E. & S.H. Gruber. 1990. Diet, feeding habits and estimates of daily ration of young lemon sharks, Negaprion brevirostris (Poey). Copeia 1990: 204–218.Google Scholar
  22. Cort73x00E9;s, E. & S.H. Gruber. 1994. Effect of ration size on growth and gross conversion efficiency of young lemon sharks, Negaprion brevirostris. J. Fish Biol. 44: 331–341.Google Scholar
  23. Economakis, A.E. & P.S. Lobel. 1998. Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Env. Biol. Fish. 51: 129–139.Google Scholar
  24. Garrick, J.A.F. & L.P. Schultz. 1963. A guide to the kinds of potentially dangerous sharks. pp. 3–60. In: P.W. Gilbert (ed.) Sharks and Survival, D. C. Heath, Boston.Google Scholar
  25. Gero, D.R. 1952. The hydrodynamic aspects of fish propulsion. Amer. Mus. Novitates 1601: 1–32.Google Scholar
  26. Goldman, K.J., S.D. Anderson, J.E. McCosker & A.P. Klimley. 1996. Temperature, swimming depth, and movements of a white shark at the South Farallon Islands, California. pp. 111–120. In: A.P. Klimley & D.G. Ainley (ed.) Great White Sharks: The Biology of Carcharodon carcharias, Academic Press, San Diego.Google Scholar
  27. Goldman, K.J. & S.D. Anderson. 1999. Space utilization and swimming depth of white sharks, Carcharodon carcharias, at the South Farallon Islands, central California. Env. Biol. Fish. 56: 351–364.Google Scholar
  28. Goodenough, J., B. McGuire & R.A. Wallace. 1993. Perspectives on animal behavior. John Wiley & Sons, New York. 762 pp.Google Scholar
  29. Graham, J.B., H. Dewar, N.C. Lai, W.R. Lowell & S.M. Arce. 1990. Aspects of shark swimming performance determined using a large water tunnel. J. Exp. Biol. 151: 175–192.Google Scholar
  30. Gruber, S.H. 1982. Role of the lemon shark, Negaprion brevirostris (Poey) as a predator in the tropical marine environment: a multidisciplinary study. Florida Sci. 45: 4–75.Google Scholar
  31. Gruber, S.H. & J.S. Cohen. 1978. Vision in sharks. pp. 11–105. In: E. Hodgson & R. Mathewson (ed.) Sensory Biology of Sharks, Skates, and Rays, Off. Naval Res., Arlington.Google Scholar
  32. Gruber, S.H., D.R. Nelson & J.F. Morrissey. 1988. Patterns of activity and space utilization of lemon sharks, Negaprion brevirostris, in a shallow Bahamian lagoon. Bull. Mar. Sci. 43: 61–76.Google Scholar
  33. Gunn, J.S., J.D. Stevens, T.L.O. Davis & B.M. Norman. 1999. Observations on the short-term movements and behaviour of whale sharks (Rhincodon typus) at Ningaloo Reef, Western Australia. Mar. Biol. 135: 553–559.Google Scholar
  34. Hamilton, W. J. & K. E. Watts. 1970. Refuging. Ann. Rev. Ecol. Syst. 1: 263–287.Google Scholar
  35. Helfman, G.S. 1993. Fish behaviour by day, night and twilight. pp. 479–512. In: T.J. Pitcher (ed.) Behaviour of Teleost Fishes, Chapman & Hall, London.Google Scholar
  36. Holland, K.N., C.G. Lowe, J.D. Peterson & A. Gill. 1992. Tracking coastal sharks with small boats: hammerhead shark pups as a case study. Aust. J. Mar. Freshwat. Res. 43: 61–66.Google Scholar
  37. Holland, K.N., B.M. Wetherbee, C.G. Lowe & C.G. Meyer. 1999. Movements of tiger sharks (Galeocerdo cuvier) in coastal Hawaiian waters. Mar. Biol. 134: 665–673.Google Scholar
  38. Holland, K.N., B.M. Wetherbee, J.D. Peterson & C.G. Lowe. 1993. Movements and distribution of hammerhead shark pups on their natal grounds. Copeia 1993: 495–502.Google Scholar
  39. Holts, D.B. & D.W. Bedford. 1993. Horizontal and vertical movements of the shortfin mako shark, Isurus oxyrinchus, in the southern California Bight. Aust. J. Mar. Freshwat. Res. 44: 901–909.Google Scholar
  40. Huish, M.T. & C. Benedict. 1978. Sonic tracking of dusky sharks in the Cape Fear River, North Carolina. J. Elisha Mitchell Scien. Soc. 93: 21–26.Google Scholar
  41. Kalmijn, A.J. 1978. Experimental evidence of geomagnetic orientation in elasmobranch fishes. pp. 347–353. In: K. Schmidt- Koenig & W.T. Keeton (ed.) Animal Migration, Navigation, and Homing, Springer-Verlag, Heidelberg.Google Scholar
  42. Kalmijn, A.J. 1988. Detection of weak electric fields. pp. 151–186. In: A.J. Kalmijn, J. Atama, R.R. Fay, A.N. Popper & W.N. Tavola (ed.) Sensory Biology of Aquatic Animals, Springer-Verlag, Heidelberg.Google Scholar
  43. Klimley, A.P. 1993. Highly directional swimming by scalloped hammerhead sharks, Sphyrna lewini, and subsurface irradiance, temperature, bathymetry, and geomagnetic field. Mar. Biol. 117: 1–22.Google Scholar
  44. Klimley, A.P. & S.B. Butler. 1988. Immigration and emigration of a pelagic fish assemblage to seamounts in the Gulf of California related to water mass movements using satellite imagery. Mar. Ecol. Prog. Ser. 49: 11–20.Google Scholar
  45. Klimley, A.P., S.B. Butler, D.R. Nelson & A.T. Stull. 1988. Diel movement of scalloped hammerhead shark, Sphyrna lewini Griffith and Smith, to and from a seamouth in the Gulf of California. J. Fish Biol. 33: 751–761.Google Scholar
  46. Klimley, A.P., I. Cabrera-Mancilla & J.L. Castillo-Geniz. 1993. Horizontal and vertical movements of the scalloped hammerhead shark, Sphyrna lewini, in the southern Gulf of California, Mexico. Ciencias Marinas 19: 95–115.Google Scholar
  47. Klimley, A.P. & D.R. Nelson. 1984. Diel movement patterns of the scalloped hammerhead shark (Sphyrna lewini) in relation to El Bajo Espiritu Santo: a refuging central-position social system. Behav. Ecol. Sociobiol. 15: 45–54.Google Scholar
  48. Lowe, C.G. & K.J. Goldman. 2001. Thermal and bioenergetics of elasmobranchs: bridging the gap. Env. Biol. Fish. 60: 251–266.Google Scholar
  49. Lowe, C.G., K. N. Holland & T.G. Wolcott. 1998. A new acoustic tail beat transmitter for fishes. Fish. Res. 36: 275–283.Google Scholar
  50. Major, P.F. 1977. Predator-prey interactions in schooling fishes during periods of twilight: a study of the silverside Pranesus insularum in Hawaii. U.S. Fish. Bull. 75: 425–426.Google Scholar
  51. Matern, S.A., J.J. Cech & T.E. Hopkins. 2000. Diel movements of bat rays, Myliobatis californica, in Tomales Bay, California: evidence for behavioral thermoregulation? Env. Biol. Fish. 58: 171–180.Google Scholar
  52. McCosker, J.E. 1987. The white shark, Carcharodon carcharias, has a warm stomach. Copeia 1987: 195–197.Google Scholar
  53. McKibben, J.N. & D.R. Nelson. 1986. Patterns of movement and groupings of grey reef sharks, Carcharhinus amblyrhynchos, at Eniwetak, Marshall Islands. Bull. Mar. Sci. 38: 89–110.Google Scholar
  54. Medved, R.J. & J.A. Marshall. 1983. Short-term movements of young sandbar sharks, Carcharhinus plumbeus. Bull. Mar. Sci. 33: 87–93.Google Scholar
  55. Metcalfe, J.D., G.P. Arnold & P.W. Webb. 1990. The energetics of migration by selective tidal stream transport: an analysis for plaice tracked in the southern North Sea. J. Mar. Biol. Ass. U.K. 70: 149–162.Google Scholar
  56. Morrissey, J.F. & S.H. Gruber. 1993a. Habitat selection by the juvenile lemon shark, Negaprion brevirostris. Env. Biol. Fish. 38: 311–319.Google Scholar
  57. Morrissey, J.F. & S.H. Gruber. 1993b. Home range of juvenile lemon sharks, Negaprion brevirostris. Copeia 1993: 425–434.Google Scholar
  58. Myrberg, A.A. Jr. 1976. Behavior of sharks - a continuing enigma. Nav. Res. Rev. 29: 1–11.Google Scholar
  59. Nelson, D.R., J.N. McKibben, W.R. Strong, Jr., C.G. Lowe, J.A. Sisneros, D.M. Schroeder & R.J. Lavenberg. 1997. An acoustic tracking of a megamouth shark, Megachasma pelagios: a crepuscular vertical migrator. Env. Biol. Fish. 49: 389–399.Google Scholar
  60. Nixon, A.J. & S.H. Gruber. 1988. Diel metabolic and activity patterns of the lemon shark (Negaprion brevirostris). J. Exp. Zool. 248: 1–6.Google Scholar
  61. Parsons, G.R. & J.K. Carlson. 1998. Physiological and behavioral responses to hypoxia in the bonnethead shark, Sphyrna tiburo: routine swimming and respiratory regulation. Fish Phys. Biochem. 19: 189–196.Google Scholar
  62. Priede, I.G. 1984.A basking shark (Cetorhinus maximus) tracked by satellite together with simultaneous remote sensing. Fish. Res. 2: 201–216.Google Scholar
  63. Rogers, S.C., D.W. Church, A.H. Weatherly & D.G. Pincock. 1984. An automated ultrasonic telemetry system for the assessment of locomotor activity in free-ranging rainbowtrout, Salmo gairdneri Richardson. J. Fish Biol. 25: 697–710.Google Scholar
  64. Scharold, J. & S.H. Gruber. 1991. Telemetered heart rate as a measure of metabolic rate in the lemon shark, Negaprion brevirostris. Copeia 1991: 942–953.Google Scholar
  65. Sciarrotta, T.C. & D.R. Nelson. 1977. Diel behavior of the blue shark, Prionace glauca, near Santa Catalina Island, California. U.S. Fish. Bull. 75: 519–528.Google Scholar
  66. Silliman, W.R. & S.H. Gruber. 1999. Behavioral biology of the spotted eagle ray, Aetobatus narinari (Euphrasen, 1790), in Bimini, Bahamas; an interim report. Bahamas J. Sci. 7: 13–20.Google Scholar
  67. Sims, D.W. 1999. Threshold foraging behaviour of basking sharks on zooplankton: life on an energetic knife-edge? Proc. R. Soc. Lond. B 266: 1437–1443.Google Scholar
  68. Standora, E.A. & D. R. Nelson. 1977. A telemetric study of the behavior of free-swimming Pacific angel sharks, Squatina californica. Bull. South. Cal. Acad. Sci. 76: 193–201.Google Scholar
  69. Strong, W.R., Jr., B.D. Bruce, D.R. Nelson & R.D. Murphy. 1996. Population dynamics of white sharks in Spencer Gulf, South Australia. pp. 401–414. In: A.P. Klimley & D.G. Ainley (ed.) Great White Sharks: The Biology of Carcharodon carcharias, Academic Press, San Diego.Google Scholar
  70. Strong, W.R., Jr., R.D. Murphy, B.D. Bruce & D.R. Nelson. 1992. Movements and associated observations of bait-attracted white sharks, Carcharodon carcharias: a preliminary report. Aust. J. Mar. Freshwat. Res. 43: 13–20.Google Scholar
  71. SundstrÖm, L.F. & S.H. Gruber. 1998. Using speed sensing transmitters to model the bioenergetics of subadult lemon sharks, Negaprion brevirostris (Poey), in the field. Hydrobiol. 271/272: 241–247.Google Scholar
  72. SundstrÖm, L.F., J. Sterk & S.H. Gruber. 1998. Effects of a speedsensing transmitter on the swimming speed of lemon sharks. Bahamas J. Sci. 6: 12–22.Google Scholar
  73. Swihart, R.K. & N.A. Slade. 1985. Testing for independence of observations in animal movements. Ecology 66: 1176–1184.Google Scholar
  74. Thomson, K.S. & D.E. Simanek. 1977. Body form and locomotion in sharks. Amer. Zool. 17: 343–354.Google Scholar
  75. Thorson, T.B. 1971. Movement of bull sharks, Carcharhinus leucas, between the Caribbean Sea and Lake Nicaragua demonstrated by tagging. Copeia 1971: 336–339.Google Scholar
  76. Tricas, T.C. & J.E. McCosker. 1984. Predatory behavior of the white shark, Carcharodon carcharias, with notes on its biology. Proc. Calif. Acad. Sci. 14: 221–238.Google Scholar
  77. Tricas, T.C., L.R. Taylor & G. Naftel. 1981.Diel behavior of the tiger shark, Galeocerdo cuvier, at French Frigate Schoals, Hawaiian Islands. Copeia 1981: 904–908.Google Scholar
  78. Voegeli, F.A., M.J. Smale, D.M. Webber, Y. Andrade & R.K. O'Dor. 2001. Ultrasonic telemetry, tracking and automated monitoring technology for sharks. Env. Biol. Fish. 60: 267–281.Google Scholar
  79. Webb, P.W. 1984. Form and function in fish swimming. Sci. Amer. 241: 72–82.Google Scholar
  80. Webb, P.W. & R.S. Keyes. 1982. Swimming kinematics of sharks. U.S. Fish. Bull. 80: 803–812.Google Scholar
  81. Wiltschko, R. & W. Wiltschko. 1995. Magnetic Orientation in Animals. Springer-Verlag, Heidelberg. 297 pp.Google Scholar
  82. Wood, G.L. 1982. The Guinness book of animal facts and feats. G.L.Woods and Guinness Superlatives LTD, New York. 275 pp.Google Scholar
  83. Yano, K. & S. Tanaka. 1986. A telemetric study on the movements of the deep sea squaloid shark, Centrophorus acus. pp. 372–380. In: T. Uyeno, R. Arai, T. Taniuchi & K. Matsuura (ed.) Indo-Pacific Fish Biology, The Ichthyological Soc. Japan, Tokyo.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • L. Fredrik Sundström
    • 1
  • Samuel H. Gruber
    • 2
  • Susi M. Clermont
    • 3
  • João P.S. Correia
    • 4
  • Jean R.C. de Marignac
    • 5
  • John F. Morrissey
    • 6
  • Courtney R. Lowrance
    • 7
  • Lori Thomassen
    • 8
  • Miguel T. Oliveira
    • 4
  1. 1.Department of ZoologyGöteborg University, Animal EcologyGöteborgSweden
  2. 2.Bimini Biological Field StationUniversity of Miami, Rosenstiel School of Marine and Atmospheric ScienceMiamiU.S.A.
  3. 3.Zoological InstituteUniversity of CopenhagenCopenhagenDenmark
  4. 4.Oceanário de LisboaLisboaPortugal
  5. 5.Moss Landing Marine LaboratoriesU.S.A.
  6. 6.Department of BiologyHempsteadU.S.A.
  7. 7.Department of Biological SciencesFlorida Institute of TechnologyMelbourneU.S.A.
  8. 8.SeaWorld of FloridaOrlandoU.S.A.

Personalised recommendations