Skip to main content
SpringerLink
Log in

Biochemical indices of aerobic and anaerobic capacity in muscle tissues of California elasmobranch fishes differing in typical activity level

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Biochemical indices of aerobic and anaerobic metabolic capacity were measured in white myotomal muscle of eight marine elasmobranch fish species representing a broad range of locomotor performance, and in red myotomal muscle and heart of three of those species. The objectives were to determine if metabolic capacities vary with typical fish activity level, to compare the endothermic mako shark with ectothermic pelagic sharks, and to compare elasmobranchs with teleosts in order to test the hypothesis that elasmobranchs have lower aerobic capacities, metabolic rates, and swimming speeds. In white myotomal muscle, activities of the enzymes citrate synthase (an index of aerobic capacity), pyruvate kinase, and lactate dehydrogenase (LDH, an index of anaerobic capacity) covaried with typical activity level, and the ability to tolerate intracellular acidification (nonbicarbonate buffering capacity) corresponded with LDH activity. Enzyme activities in red muscle and heart did not show a consistent pattern with respect to fish activity. In comparison with ectothermic sharks, the mako shark had greater aerobic and anaerobic capacities in white muscle, but no significant differences were found in red muscle or heart. This pattern has also been found in teleosts. Thus, endothermic fishes elevate the temperature of red muscle, a tissue specialized for high aerobic performance, whereas white muscle biochemical characteristics are adjusted to support high rates of contraction both aerobically and anaerobically. Muscle enzymic activities of elasmobranchs and teleosts with comparable locomotor habits are similar, thus refuting the hypothesis that elasmobranchs are sluggish, with lower metabolic capacities than teleosts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Abe, H., Dobson, G. P., Hoeger, U., Parkhouse, W. S. (1985). Role of histidine-related compounds to intracellular buffering in fish skeletal muscle. Am. J. Physiol. 249: R449-R454

    Google Scholar 

  • Alp, P. R., Newsholme, E. A., Zammit, V. A. (1976). Activities of citrate synthase and NAD+-linked and NADP+-linked isocitrate dehydrogenase in muscle from vertebrates and invertebrates. Biochem. J. 154: 689–700

    Google Scholar 

  • Ballantyne, J. S., Chamberlin, M. E., Singer, T. D. (1992). Oxidative metabolism in thermogenic tissues of the swordfish and mako shark. J. exp. Zool. 261: 110–114

    Google Scholar 

  • Beamish, F. W. H. (1978). Swimming capacity. In: Hoar, W. S., Randall, D. J. (eds.) Fish physiology. Vol. VII. Academic Press, New York, p. 101–187

    Google 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. Elsevier, New York, p. 269–311

    Google Scholar 

  • Bone, Q. (1978). Locomotor muscle. In: Hoar, W. S., Randall, D. J. (eds.) Fish physiology. Vol VII. Academic Press, New York, p. 361–424

    Google Scholar 

  • Bone, Q. (1988). Muscles and locomotion. In: Shuttleworth, T. J. (ed.) Physiology of elasmobranch fishes. Springer-Verlag, New York, p. 99–141

    Google Scholar 

  • Bone, Q., Kiceniuk, J., Jones, D. R. (1978). On the role of the different fiber types in fish myotomes at intermediate swimming speeds. Fish. Bull. U.S. 34: 294–301

    Google Scholar 

  • Brett, J. R., Blackburn, J. M. (1978). Metabolic rate and energy expenditure of the spiny dogfish, Squalus acanthias. J. Fish. Res. Bd Can. 35: 816–821

    Google Scholar 

  • Bushnell, P. G., Lutz, P. L., Gruber, S. H. (1989). The metabolic rate of an active, tropical elasmobranch, the lemon shark (Negaprion brevirostris). Expl Biol. 48: 279–283

    Google Scholar 

  • Carey, F. G., Casey, J. G., Pratt, H. L., Urquhart, D., McCosker, J. E. (1985). Temperature, heat production, and heat exchange in lamnid sharks. Mem. sth. Calif. Acad. Sci. 9: 92–108

    Google Scholar 

  • Carey, F. G., Scharold, J. V. (1990). Movements of blue sharks (Prionace glauca) in depth and course. Mar. Biol. 106: 329–342

    Google Scholar 

  • Carey, F. G., Teal, J. M. (1969). Mako and porbeagle: warm-bodied sharks. Comp. Biochem. Physiol. 28: 199–204

    Google Scholar 

  • Carey, F. G., Teal, J. M., Kanwisher, J. W., Lawson, K. D., Beckett, J. S. (1971). Warm-bodied fishes. Am. Zool. 11: 135–143

    Google Scholar 

  • Castellini, M. A., Somero, G. N. (1981). Buffering capacity of vertebrate muscle: correlations with potentials for anaerobic function. J. comp. Physiol. 143: 191–198

    Google Scholar 

  • Childress, J. J., Somero, G. N. (1979). Depth-related enzymic activities in muscle, brain and heart of deep-living pelagic marine teleosts. Mar. Biol. 52: 273–283

    Google Scholar 

  • Cliff, G., Thurman, G. D. (1984). Pathological and physiological effects of stress during capture and transport in the juvenile dusky shark, Carcharhinus obscurus. Comp. Biochem. Physiol. 78A: 167–173

    Google Scholar 

  • Crabtree, B., Newsholme, E. A. (1972). The activities of lipases and carnitine palmitoyltransferase in muscle from vertebrates and invertebrates. Biochem. J. 130: 697–705

    Google Scholar 

  • Dickson, K. A. (1988). Why are some fishes endothermic? Interspecific comparisons of aerobic and anaerobic metabolic capacities in endothermic and ectothermic scombrids. Ph. D. dissertation. University of California at San Diego

  • Dickson, K. A. (1993). Unique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment. Devs envirl Biol. Fish. (in press)

  • Dickson, K. A., Dall, A. V., Eisman, J. M., McDonnell, E. T., Hendrzak, A. M. (1988). Biochemical indices of aerobic and anaerobic capacity in red and white myotomal muscle of active, pelagic sharks: comparisons between endothermic and ectothermic species. J. Pa Acad. Sci. 62: 147–151

    Google Scholar 

  • Dickson, K. A., Somero, G. N. (1987). Partial characterization of the buffering components of the red and white myotomal muscle of marine teleosts, with special emphasis on scombrid fishes. Physiol. Zoöl. 60: 699–706

    Google Scholar 

  • Dobson, G. P., Wood, S. C., Daxboeck, C., Perry, S. F. (1986). Intracellular buffering and oxygen transport in the Pacific blue marlin (Makaira nigricans): adaptations to high-speed swimming. Physiol. Zoöl. 59: 150–156

    Google Scholar 

  • Evans, D. H. (1982). Mechanisms of acid extrusion by two marine fishes: the teleost, Opsanus beta, and the elasmobranch, Squalus acanthias. J. exp. Biol. 97: 289–299

    Google Scholar 

  • Ewart, H. S., Driedzic, W. R. (1987). Enzymes of energy metabolism in salmonid hearts: spongy versus cortical myocardia. Can. J. Zool. 65: 623–627

    Google Scholar 

  • Farrell, A. P. (1991). From hagfish to tuna: a perspective on cardiac function in fish. Physiol. Zoöl. 64: 1137–1164

    Google Scholar 

  • Graham, J. B. (1983). Heat transfer. In: Webb, P. W., Weihs, D. (eds.) Fish biomechanics. Praeger Publishers, New York, p. 248–279

    Google Scholar 

  • Graham, J. B., Dewar, H., Lai, N. C., Lowell, W. R., Arce, S. M. (1990). Aspects of shark swimming performance determined using a large water tunnel. J. exp. Biol. 151: 175–192

    Google Scholar 

  • Graham, J. B., Koehrn, F. J., Dickson, K. A. (1983). Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to endothermy. Can. J. Zool. 61: 2087–2096

    Google Scholar 

  • Greer Walker, M., Pull, G. A. (1975). A survey of red and white muscle in marine fish. J. Fish Biol. 7: 295–300

    Google Scholar 

  • Gruber, S. J. (1992). The effects of endurance training on the leopard shark, Triakis semifasciata. M.A. thesis. California State University at Fullerton

  • Gruber, S. J., Lockridge, K., Dickson, K. A. (1990). Comparisons of muscle aerobic and anaerobic capacity in endothermic and ectothermic shark species. Proceedings of the 70th Annual Meeting of the American Society of Ichthyologists and Herpetologists, June 14–20, 1990. American Society of Ichthyologists and Herpetologists. Charleston, S. Carolina, p. 95

    Google Scholar 

  • Guppy, M., Hulbert, W. C., Hochachka, P. W. (1979). Metabolic sources of heat and power in tuna muscles. II. Enzyme and metabolite profiles. J. exp. Biol. 82: 303–320

    Google Scholar 

  • Heisler, N. (1988). Acid-base regulation. In: Shuttleworth, T. J. (ed.) Physiology of elasmobranch fishes. Springer-Verlag, New York, p. 215–252

    Google Scholar 

  • Holeton, G. F., Heisler, N. (1983). Contribution of net ion transfer mechanisms to acid-base regulation after exhausting activity in the larger spotted dogfish (Scyliorhinus stellaris). J. exp. Biol. 103: 31–46

    Google Scholar 

  • Johnston, I. A. (1981). Structure and function of fish muscles. Symp. zool. Soc. Lond. 48: 71–113

    Google Scholar 

  • Johnston, I. A., Brill, R. (1984). Thermal dependence of contractile properties of single skinned muscle fibres from Antarctic and various warm water marine fishes including skipjack tuna (Katsuwonus pelamis) and kawakawa (Euthynnus affinis). J. comp. Physiol. (Sect. B) 155: 63–70

    Google Scholar 

  • Johnston, I. A., Davison, W., Goldspink, G. (1977). Energy metabolism of carp swimming muscles. J. comp. Physiol. 114: 203–216

    Google Scholar 

  • Johnston, I. A., Moon, T. W. (1980a). Endurance exercise training in the fast and slow muscles of a teleost fish (Pollachius virens). J. comp. Physiol. 135: 147–156

    Google Scholar 

  • Johnston, I. A., Moon, T. W. (1980b). Exercise training in skeletal muscle of brook trout (Salvelinus fontinalis). J. exp. Biol. 87: 177–194

    Google Scholar 

  • Johnston, I. A., Moon, T. W. (1981). Fine structure and metabolism of multiply innervated fast muscle fibres in teleost fish. Cell Tissue Res. 219: 93–109

    Google Scholar 

  • Jørgensen, J. B., Mustafa, T. (1980). The effect of hypoxia on carbohydrate metabolism in flounder (Platichthys flesus L.). II. High energy phosphate compounds and the role of glycolytic and gluconeogenetic enzymes. Comp. Biochem. Physiol. 67B: 249–256

    Google Scholar 

  • Lindsey, C. C. (1978). Form, function, and locomotory habits in fish. In: Hoar, W. S., Randall, D. J. (eds.) Fish Physiology. Vol. VII. Academic Press, New York, p. 1–100

    Google Scholar 

  • Lukton, A., Olcott, H. S. (1958). Content of free imidazole compounds in muscle tissue of aquatic animals. Fd Res. 23: 611–618

    Google Scholar 

  • Magnuson, J. J. (1978). Locomotion by scombrid fishes. In: Hoar, W. S., Randall, D. J. (eds.) Fish physiology. Vol. VII. Academic Press, New York, p. 239–313

    Google Scholar 

  • McLaughlin, R. L., Kramer, D. L. (1991). The association between amount of red muscle and mobility in fishes: a statistical evaluation. Envir. Biol. Fish. 30: 369–378

    Google Scholar 

  • Milligan, C. L., Wood, C. M. (1986). Intracellular and extracellular acid-base status and H+ exchange with the environment after exhaustive exercise in the rainbow trout. J. exp. Biol. 123: 93–121

    Google Scholar 

  • Moon, T. W., Mommsen, T. P. (1987). Enzymes of intermediary metabolism in tissues of the little skate, Raja erinacea. J. exp. Zool. 244: 9–15

    Google Scholar 

  • Moyes, C. D., Buck, L. T., Hochachka, P. W. (1990). Mitochondrial and peroxisomal fatty acid oxidation in elasmobranchs. Am. J. Physiol. 258: R756-R762

    Google Scholar 

  • Moyes, C. D., Mathieu-Costello, O. A., Brill, R. W., Hochachka, P. W. (1992). Mitochondrial metabolism of cardiac and skeletal suscles from a fast (Katsuwonus pelamis) and a slow (Cyprinus carpio) fish. Can. J. Zool. 70: 1246–1253

    Google Scholar 

  • Okuma, E., Abe, H. (1992). Major buffering constituents in animal muscle. Comp. Biochem. Physiol. 102A: 37–41

    Google Scholar 

  • Parsons, G. R. (1990). Metabolism and swimming efficiency of the bonnethead shark Sphyrna tiburo. Mar. Biol. 104: 363–367

    Google Scholar 

  • Rome, L. C., Swank, D. (1992). The influence of temperature on power output of scup red muscle during cyclical length changes. J. exp. Biol. 171: 261–281

    Google Scholar 

  • Santer, R. M. (1985). Morphology and innervation of the fish heart. Adv. Anat. Embryol. Cell Biol. 89: 1–102

    Google Scholar 

  • Scharold, J., Lai, N. C., Lowell, W. R., Graham, J. B. (1989). Metabolic rate, heart rate, and tailbeat frequency during sustained swimming in the leopard shark Triakis semifasciata. Expl Biol. 48: 223–230

    Google Scholar 

  • Sciarrotta, T. C., Nelson, D. R. (1977). Diel behavior of the blue shark, Prionace glauca, near Santa Catalina Island, California. Fish. Bull. U.S. 75: 519–528

    Google Scholar 

  • Sidell, B. D., Driedzic, W. R., Stowe, D. B., Johnston, I. A. (1987). Biochemical correlates of power development and metabolic fuel preferenda in fish hearts. Physiol. Zoöl. 60: 221–232

    Google Scholar 

  • Siebenaller, J. F., Somero, G. N. (1982). The maintenance of different enzyme activity levels in congeneric fishes living at different depths. Physiol. Zoöl. 55: 171–179

    Google Scholar 

  • Siebenaller, J. F., Somero, G. N., Haedrich, R. L. (1982). Biochemical characteristics of macrourid fishes differing in their depth of distribution. Biol. Bull. mar. biol. Lab., Woods Hole 163: 240–249

    Google Scholar 

  • Slyke, van, D. D. (1922). On the measurement of buffer values and on the relationship of buffer value to the dissociation constant of the buffer and the concentration and reaction of the buffer solution. J. biol. Chem. 52: 525–570

    Google Scholar 

  • Somero, G. N., Childress, J. J. (1980). A violation of the metabolismsize scaling paradigm: activities of glycolytic enzymes in muscle increase in larger-size fishes. Physiol. Zoöl. 53: 322–337

    Google Scholar 

  • Somero, G. N., Childress, J. J. (1990). Scaling of ATP-supplying enzymes, myofibrillar proteins and buffering capacity in fish muscle: relationship to locomotory habit. J. exp. Biol. 149: 319–333

    Google Scholar 

  • Suarez, R. K., Mallet, M. D., Daxboeck, C., Hochachka, P. W. (1986). Enzymes of energy metabolism and gluconeogenesis in the Pacific blue marlin Makaira nigricans. Can. J. Zool. 64: 694–697

    Google Scholar 

  • Sullivan, K. M., Somero, G. N. (1980). Enzyme activities of fish skeletal muscle and brain as influenced by depth of occurrence and habits of feeding and locomotion. Mar. Biol. 60: 91–99

    Google Scholar 

  • Swift, D. J. (1983). Blood component value changes in the Atlantic mackerel (Scomber scombrus L.) subjected to capture, handling, and confinement. Comp. Biochem. Physiol. 76A: 795–802

    Google Scholar 

  • Torres, J. J., Somero, G. N. (1988). Metabolism, enzymic activities and cold adaptation in Antarctic mesopelagic fishes. Mar. Biol. 98: 169–180

    Google Scholar 

  • Tota, B. (1983). Vascular and metabolic zonation in the ventricular myocardium of mammals and fishes. Comp. Biochem. Physiol. 76A: 423–437

    Google Scholar 

  • Tullis, A., Block, B. A., Sidell, B. D. (1991). Activities of key metabolic enzymes in the heater organs of scombroid fishes. J. exp. Biol. 161: 383–403

    Google Scholar 

  • Wells, R. M. G., Davie, P. S. (1985), Oxygen binding by the blood and hematological effects of capture stress in two big gamefish: mako shark and striped marlin. Comp. Biochem. Physiol. 81A: 643–646

    Google Scholar 

  • Wood, C. M. (1991). Acid-base and ion balance, metabolism, and their interactions, after exhaustive exercise in fish. J. exp. Biol. 160: 285–308

    Google Scholar 

  • Yancey, P. H., Clark, M. E., Hand, S. C., Bowlus, D., Somero, G. N. (1982). Living with water stress: evolution of osmolyte systems. Science, N.Y. 217: 1214–1222

    Google Scholar 

  • Yancey, P. H., Somero, G. N. (1980). Methylamine osmoregulatory solutes of elasmobranch fishes counteract urea inhibition of enzymes. J. exp. Zool. 212: 205–213

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Science, California State University at Fullerton, 92634-9480, Fullerton, California, USA

    K. A. Dickson, M. O. Gregorio, S. J. Gruber, K. L. Loefler, M. Tran & C. Terrell

Authors
  1. K. A. Dickson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. O. Gregorio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. J. Gruber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. L. Loefler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Tran
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Terrell
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by M. G. Hadfield, Honolulu

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dickson, K.A., Gregorio, M.O., Gruber, S.J. et al. Biochemical indices of aerobic and anaerobic capacity in muscle tissues of California elasmobranch fishes differing in typical activity level. Marine Biology 117, 185–193 (1993). https://doi.org/10.1007/BF00345662

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00345662

Keywords

Search

Navigation