Environmental Biology of Fishes

, Volume 60, Issue 1–3, pp 251–266 | Cite as

Thermal and Bioenergetics of Elasmobranchs: Bridging the Gap

  • Christopher G. Lowe
  • Kenneth J. Goldman


Physiological telemetry is a powerful tool in studying the thermal biology and energetics of elasmobranchs in the laboratory and field. Controlled laboratory studies have increased our understanding of the physiology and behavior of many elasmobranchs, but have focused primarily on small, slow moving species. Extrapolating results from these laboratory studies to free-swimming animals in the field or to other unstudied species may be problematic, due to laboratory constraints or species specific differences. Some elasmobranchs are too large or logistically difficult to maintain in captivity, making them extremely difficult to study in the laboratory, and thus can only be studied in the field. Physiological telemetry offers a ‘bridge’ between the laboratory and the field providing an opportunity to elucidate similarities and differences. Previous studies have coupled a variety of sensors with ultrasonic transmitters to relay information on epaxial muscle and stomach temperatures of free-swimming lamnid sharks. Even though these studies indicate lamnids exhibit elevated body temperatures, the degree to which these sharks may control body temperature is still not fully understood. Telemetry of heart rate, swimming speed, muscle contraction rate, and tail beat frequency has been used to estimate energy consumption of free-swimming elasmobranchs with varying success. Based on recent advances in technology, several hypotheses regarding thermoregulation, cardiac output, and obligate ram ventilation are discussed. Although many telemetry studies have been restricted by logistical difficulties in conducting long-term tracks, recent developments such as acoustic modems, underwater listening stations and satellite telemetry may significantly increase the amount and types of physiological data that can be collected. These improvements in technology and captive animal husbandry techniques will help to ‘bridge the gap’ between the laboratory and the field.

energetics thermoregulation ultrasonic telemetry transmitters 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alexander, R.L. 1995. Evidence of a counter-current heat exchanger in the ray Mobula tarapacana (Chondrichthyes: Elasmobranchii: Batiodea: Myliobatiformes). J. Zool. Lond. 237: 377–384.Google Scholar
  2. Alexander, R.L. 1996. Evidence of brain-warming in the mobulid rays, Mobula tarapacana and Manta birostris (Chondrichthyes: Elasmobranchii: Batiodea: Myliobatiformes). J. Linn. Soc. 188: 151–164.Google Scholar
  3. Armstrong, J.D. 1986. Heart rate as an indicator of activity, metabolic rate, food intake, and digestion in pike, Esox lucius. J. Fish Biol. 29: 207–221.Google Scholar
  4. Armstrong, J.D., M.C. Lucas, I.G. Priede & L. DeVera. 1989. An acoustic telemetry system for monitoring the heart rate of pike, Esox lucius L., and other fishes in their natural environment. J. Exp. Biol. 143: 549–552.Google Scholar
  5. Bainbridge, R. 1958. The speed of swimming of fish as related to size and to the frequency and amplitude of the tail beat. J. Exp. Biol. 35: 1183–1226.Google Scholar
  6. Block, B.A. & F.G. Carey. 1985.Warm brain and eye temperatures in sharks. J. Comp. Physiol. B. 156: 229–236.Google Scholar
  7. Block, B.A. & J.R. Finnerty. 1994. Endothermy in fishes: a phylogenetic analysis of constraints, predispositions, and selection pressures. Env. Biol. Fish. 40: 283–302.Google Scholar
  8. Brett, J.R. & J.M. Blackburn. 1978. Metabolic rate and energy expenditure of the spiny dogfish, Squalus acanthias. J. Fish. Res. Board Can. 35: 816–821.Google Scholar
  9. Briggs, C.T. & J.R. Post. 1997. In situ activity metabolism of rainbow trout (Oncorhynchus mykiss): estimates obtained from telemetry of axial muscle electromyograms. Can. J. Fish. Aquat. Sci. 54: 859–866.Google Scholar
  10. Brill, R.W., H. Dewar & J.B. Graham. 1994. Basic concepts relevant to heat transfer in fishes, and their use in measuring the physiological thermoregulatory abilities of tunas. Env. Biol. Fish. 40: 109–124.Google Scholar
  11. Burne, R.H. 1923. Some peculiarities of the blood vascular system of the porbeagle shark, Lamna cornubica. Phil.Trans. Roy. Soc. London 212: 209–257.Google Scholar
  12. 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
  13. Carey, F.G. & K.D. Lawson. 1973. Temperature regulation in free-swimming bluefin tuna. Comp. Biochem. Physiol. 44A: 375–392.Google Scholar
  14. Carey, F.G. 1982. A brain heater in the swordfish. Science 216: 1327–1329.Google Scholar
  15. Carey, F.G., J.G. Casey, H.L. Pratt, D. Urquhart & J.E. McCosker. 1985. Temperature, heat production, and heat exchange in lamnid sharks. Mem. So. Calif. Acad. Sci. 9: 92–108.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.W. Kanwisher & E.D. Stevens. 1984. Bluefin tuna warm their viscera during digestion. J. Exp. Biol. 109: 1–20.Google Scholar
  18. Carey, F.G. 1973. Fishes with warm bodies. Sci. Amer. 228: 36–44.Google Scholar
  19. Carey, F.G. & B.H. Robison. 1981. Daily patterns in the activities of swordfish, Xiphias gladius, observed by acoustic telemetry. U.S. Fish. Bull. 79: 277–292.Google Scholar
  20. Carey, F.G. & J. Scharold. 1990. Movements of blue sharks (Prionace glauca) in depth and course. Mar. Biol. 106: 329–342.Google Scholar
  21. Carey, F.G. & J.M. Teal. 1969. Mako and porbeagle:warm-bodied sharks. Comp. Biochem. Physiol. 28: 199–204.Google Scholar
  22. Carey, F.G., J.M. Teal, J.W. Kanwisher, K.D. Lawson & J.S. Beckett. 1971. Warm-bodied fish. Amer. Zool. 11: 137–145.Google Scholar
  23. Carey, F.G., J.M. Teal & J.W. Kanwisher. 1981. The visceral temperatures of mackerel sharks (Lamnidae). Physiol. Zool. 54: 334–344.Google Scholar
  24. Dewar, H. & J.B. Graham. 1994. Studies of tropical tuna swimming performance in a large water tunnel. III. Kinematics. J. Exp. Biol. 192: 45–59.Google Scholar
  25. Emery, S.H. 1985. Hematology and cardiac morphology in the great white shark, Carcharodon carcharias. Mem. So. Calif. Acad. Sci. 9: 73–80.Google Scholar
  26. Emery, S.H. 1986. Hematological comparisons of endothermic vs. ectothermic elasmobranch fishes. Copeia 1986: 700–705.Google Scholar
  27. Emery, S.H., C. Mangano & V. Randazzo. 1985. Ventricle morphology in pelagic elasmobranch fishes. Comp. Biochem. Physiol. 8: 635–643.Google Scholar
  28. Eschricht, D.F. & J. Müller. 1835a. Über die arteriösen and venösen Wundernetze an der Leber und einen merkwürdigen Bau dieses Organes beim Thunfische, Thynnus vulgaris. Physikal. Abhandl. d. K. Wissensch. Berlin. 32 pp. (after Fudge & Stevens 1996).Google Scholar
  29. Eschricht, D.F. & J. Müller. 1835b. Nachtrag zu der Abhandlung der Herren Eschricht und Müller über die Wundernetze an der Leber des Thunfisches. Über die Wundernetze am Darmkanal des Squalus vulpes L., Alopecias vulpes Nob. Physikal. Abhandl. d. K.Wissensch. Berlin. pp. 325–328 (after Fudge & Stevens 1996).Google Scholar
  30. Farrell, A.P. 1991. From hagfish to tuna - a perspective on cardiac function. Physiol. Zool. 64: 1137–1164.Google Scholar
  31. Farrell, A.P. & D.R. Jones. 1992. The heart. pp. 1–88. In: W.S. Hoar, D.J. Randall & A.P. Farrell (ed.) Fish Physiology, Vol. 12A, Academic Press, San Diego.Google Scholar
  32. Fudge, D.S. & E.D. Stevens. 1996. The visceral retia mirabilia of tuna and sharks: an annotated translation and discussion of the Eschricht & Müller 1835 paper and related papers. Guelph Ichthyol. Rev. 4: 1–92.Google Scholar
  33. Goldman, K.J. 1997. Regulation of body temperature in the white shark, Carcharodon carcharias. J. Comp. Physiol.B167: 423–429.Google Scholar
  34. 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: 353–366.Google Scholar
  35. 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: Ecology and Behavior, Academic Press, San Diego.Google Scholar
  36. Graham, J.B. 1983. Heat transfer. pp. 248–279. In: P.W. Webb & D. Weihs (ed.) Fish Biomechanics, Praeger Publishing, New York.Google Scholar
  37. 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
  38. Gruber, S.H. 1984. Bioenergetics of captive and free-ranging lemon sharks. AAZPA Ann. Conf. Proc.: 340–373.Google Scholar
  39. 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
  40. Hickman, C.P., L.S. Roberts & F.M. Hickman. 1984. Integrated principles of zoology. Times Mirror/Mosbey College Pub., St. Louis. 1065 pp.Google Scholar
  41. Hochachka, P.W., W.C. Hulbert & M. Guppy. 1978. The tuna power plant and furnace. pp. 153–181. In: G.D. Sharp & A.E. Dizon (ed.) The Physiological Ecology of Tunas, Academic Press, New York.Google Scholar
  42. Holland, K.N., R.W. Brill, R.K.C. Chang & R Yost. 1985.A small vessel technique for tracking pelagic fish. Mar. Fish. Rev. 47: 26–32.Google Scholar
  43. 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. Freshwater Res. 43: 61–66.Google Scholar
  44. Holland, K.N., B.M. Wetherbee, C.G. Lowe & C. Meyer. 1999. Movements of tiger sharks in coastal Hawaiian waters. Mar. Biol. 134: 665–673.Google Scholar
  45. Hunter, J.R. & J.R. Zweifel. 1971. Swimming speed, tail beat frequency, tail beat amplitude, and size in jack mackerel, Trachurus symmetricus, and other fishes. U.S. Fish. Bull. 69: 253–256.Google Scholar
  46. Jones, D.R. & D.J. Randall. 1978. The respiratory and circulatory systems during exercise. pp. 425–501. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Vol. 7, Academic Press, New York.Google Scholar
  47. Kanwisher, J.W., K. Lawson & G. Sundnes. 1974. Acoustic telemetry from fish. U.S. Fish. Bull. 72: 251–255.Google Scholar
  48. Klimley, A.P. & S.D. Anderson. 1996. Residency patterns of white sharks at the South Farallon Islands, California. pp. 365–374. In: A.P. Klimley & D.G. Ainley (ed.) Great White Sharks: Ecology and Behavior, Academic Press, San Diego.Google Scholar
  49. Kotchabhakdi, N., J. Kanwisher & C.L. Prosser. 1973. Acoustic telemetry of electrical activity from the brain of free-swimming dogfish. Biol. Bull. 145: 443–444.Google Scholar
  50. Lai, N.C., J.B. Graham, W.R. Lowell & R. Shabetai. 1989. Elevated pericardial pressure and cardiac output in the leopard shark Triakis semifasciata during exercise: the role of the pericardioperitoneal canal. J. Exp. Biol. 147: 263–277.Google Scholar
  51. Lai, N.C., K.E. Korsmeyer, S. Katz, D.B. Holts, L.M. Laughlin & J.B. Graham. 1997. Hemodynamics and blood properties of the shortfin mako shark (Isurus oxyrinchus). Copeia 1997: 424–428.Google Scholar
  52. Lowe, C.G. 1996. Kinematics and critical swimming speed of juvenile scalloped hammerhead sharks. J. Exp. Biol. 199: 2605–2610.Google Scholar
  53. Lowe, C.G., K.N. Holland & T.G. Wolcott. 1998. A new acoustic tailbeat transmitters for fishes. Fish. Res. 36: 275–283.Google Scholar
  54. Lowe, C.G. 1998. Swimming efficiency and bioenergetics of juvenile scalloped hammerhead sharks in Kaneohe Bay, Hawaii. Ph.D. Dissertation, University of Hawaii, Honolulu. 130 pp.Google Scholar
  55. Lucas, M.C., J.D. Armstrong, I.G. Priede, A.N.Z. Gindy & L. De Vera. 1991. Direct movements of metabolism, activity and feeding behaviour of pike, Esox lucius L., in the wild, by the use of heart rate telemetry. J. Fish Biol. 39: 325–345.Google Scholar
  56. Lucas, M.C., A.D.F. Johnstone & I.G. Priede. 1993. Use of physiological telemetry as a method of estimating metabolism of fish in the natural environment. Trans. Amer. Fish. Soc. 122: 822–833.Google Scholar
  57. Lutcavage, M.E., R.W. Brill, G.S. Skomal, B.C. Chase & P.W. Howey. 1999. Results of pop-up satellite tagging of spawning size class fish in the Gulf of Maine: do north Atlantic bluefin tuna spawn in the mid-Atlantic. Can. J. Fish. Aquat. Sci. 56: 173–177.Google Scholar
  58. McCosker, J.E. 1987. The white shark, Carcharodon carcharias, has a warm stomach. Copeia 1987: 195–197.Google Scholar
  59. Medved, R.J., C.E. Stillwell & J.G. Casey. 1988. The rate of food consumption of young sandbar sharks (Carcharhinus plumbeus) in Chincoteague Bay, Virginia. Copeia 1988: 956–963.Google Scholar
  60. Naylor, G.J.P., A.P. Martin, E.G. Mattison & W.M. Brown. 1997. Interrelationships of lamniform sharks: testing phylogenetic hypotheses with sequence data. pp. 199–217. In: T. Kocher & C.A. Stephien (ed.) Molecular Systematics of Fishes, Academic Press, San Diego.Google Scholar
  61. Neill, W.H., R.K. Chang & A.E. Dizon. 1976. Magnitude and ecological implications of thermal inertia in skipjack tuna, Katsuwonnus pelamis (Linnaeus). Env. Biol. Fish. 1: 61–80.Google Scholar
  62. Nelson, D.R. 1974. Ultrasonic telemetry of shark behavior. Nav. Res. Rev. 27: 1–21.Google Scholar
  63. Nelson, D.R. 1978. Telemetering techniques for the study of freeranging sharks. pp. 419–482. In: E. Hodgson & R. Mathewson (ed.) Sensory Biology of Sharks, Skates, and Rays, Off. Naval Res., Arlington.Google Scholar
  64. Nelson, D.R. 1990. Telemetry studies of sharks: a review, with applications in resource management. pp. 239–256. In: H.L. Pratt, S.H. Gruber & T. Taniuchi (ed.) Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and Status of the Fisheries, NOAA Tech. Rep. NMFS 90.Google Scholar
  65. Nelson, D.R. & R.H. Johnson. 1980. Behavior of the reef sharks of Rangiroa, French Polynesia. Natl. Geogr. Soc. Res. Rep. 12: 479–499.Google Scholar
  66. Parsons, G.R. 1990. Metabolism and swimming efficiency of the bonnethead shark Sphyrna tiburo. Mar. Biol. 104: 363–367.Google Scholar
  67. 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 Physiol. Biochem. 19: 189–196.Google Scholar
  68. Priede, I.G. 1984. A basking shark (Cetorhinus maximus) tracked by satellite together with simultaneous remote sensing. Fish. Res. 2: 201–216.Google Scholar
  69. Priede, I.G. & A.H. Young. 1977. Ultrasonic telemetry of cardiac rhythms of wild brown trout (Salmo trutta, L.) J. Fish Biol. 10: 299–318.Google Scholar
  70. Pritchard, A.W., E. Florey & A.W. Martin. 1958. Relationship between metabolic rate and body size in an elasmobranch (Squalus suckleyi) and in a teleost (Ophiodon elongatus). J. Mar. Res. 17: 403–411.Google Scholar
  71. Weatherley, A.H., P.A. Kaselo, M.D. Gare, J.M. Gunn & B. Lipicnik. 1996. Field activity of lake trout during the reproductive period monitored by electrogram telemetry. J. Fish Biol. 48: 647–685.Google Scholar
  72. Ross, L.G., W. Watts & A.H. Young. 1981. An ultrasonic biotelemetry system for the continuous monitoring of tail-beat rate from free-swimming fish. J. Fish Biol. 18: 479–490.Google Scholar
  73. 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
  74. Scharold, J., N.C. Lai, W.R. Lowell & J.B. Graham. 1989. Metabolic rate, heart rate, and tailbeat frequency during sustained swimming in the leopard shark Triakis semifasciata. Exp. Biol. 48: 223–230.Google Scholar
  75. Smith, R.L. & D. Rhodes. 1983. Body temperature of the salmon shark, Lamna ditropis. J. Mar. Biol. Ass. U.K. 63: 243–244.Google Scholar
  76. Stasko, A.B. & R.M. Horrall. 1976. Method of counting tailbeats of free-swimming fish by ultrasonic telemetry techniques. J. Fish. Res. Board Can. 33: 2596–2598.Google Scholar
  77. Stillwell, C.E. & N.E. Kohler. 1982. Food, feeding habits, and estimates of daily ration of the shortfin mako (Isurus oxyrinchus) in the Northwest Atlantic. Can. J. Fish. Aquat. Sci. 39: 407–414.Google Scholar
  78. Sundström, L.F. & S.H. Gruber. 1998. Using speed-sensing transmitters to construct a bioenergetics model for subadult lemon sharks, Negaprion brevirostris (Poey), in the field. Hydrobiologia 371/372: 241–247.Google Scholar
  79. Toda, B. & A. Gattuso. 1996. Heart ventricle pumps in teleosts and elasmobranchs: a morphodynamic approach. J. Exp. Zool. 275: 162–171Google Scholar
  80. Tricas, T.C. & J.E. McCosker. 1984. Predatory behavior of the white shark (Carcharodon carcharias), with notes on its biology. Proc. Calif. Acad. Sci.43: 221–238.Google Scholar
  81. Vander, A.J., J.H. Sherman & D.S. Luciano. 1990. Human physiology: the mechanisms of body function. McGraw-Hill Publishing, New York. 145 pp.Google Scholar
  82. Voegeli, F., M.J. Smale, D.M. Webber, Y. Andrade & R. O'Dor. 2000. Ultrasonic telemetry, tracking and automated monitoring technology for sharks. Env. Biol. Fish. (in press).Google Scholar
  83. Wardle, C.S. & J.W. Kanwisher. 1974. The significance of heart rate in free swimming cod, Gadus morhua: some observations with ultra-sonic tags. Mar. Behav. Physiol. 2: 311–324.Google Scholar
  84. Webber, D.M., R.G. Boutilier & S.R. Kerr. 1998. Cardiac output as a predictor of metabolic rate in cod Gadus morhua. J. Exp. Biol. 201: 2779–2789.Google Scholar
  85. Weihs, D. 1973. Mechanically efficient swimming techniques for fish with negative buoyancy. J. Mar. Res. 31: 194–209.Google Scholar
  86. Winberg, G.G. 1956. Rate of metabolism and food requirements of fishes. Fish. Res. Board Can. Transl. Ser. No. 194, 1960: 1–253.Google Scholar
  87. Wolf, N.G., P.R. Swift & F.G. Carey. 1988. Swimming muscle helpswarm the brain of lamnid sharks. J. Comp. Physiol. B157: 709–715.Google Scholar
  88. Young, A.H., P. Tyler, F.G.T. Holliday & A. MacFarlane. 1972. A small sonic tag for measurement of locomotor activity in fish. J. Fish Biol. 4: 57–65Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Christopher G. Lowe
    • 1
  • Kenneth J. Goldman
    • 2
  1. 1.Department of Biological SciencesCalifornia State University, Long BeachLong BeachU.S.A.
  2. 2.The College of William and Mary, School of Marine ScienceVirginia Institute of Marine ScienceGloucester PointU.S.A.

Personalised recommendations