Skip to main content

Exercise and recovery metabolism in the pacific spiny dogfish (Squalus acanthias)


We examined the effects of exhaustive exercise and post-exercise recovery on white muscle substrate depletion and metabolite distribution between white muscle and blood plasma in the Pacific spiny dogfish, both in vivo and in an electrically stimulated perfused tail-trunk preparation. Measurements of arterial-venous lactate, total ammonia, β-hydroxybutyrate, glucose, and l-alanine concentrations in the perfused tail-trunk assessed white muscle metabolite fluxes. Exhaustive exercise was fuelled primarily by creatine phosphate hydrolysis and glycolysis as indicated by 62, 71, and 85% decreases in ATP, creatine phosphate, and glycogen, respectively. White muscle lactate production during exercise caused a sustained increase (~12 h post-exercise) in plasma lactate load and a short-lived increase (~4 h post-exercise) in plasma metabolic acid load during recovery. Exhaustive exercise and recovery did not affect arterial PO2, PCO2, or PNH3 but the metabolic acidosis caused a decrease in arterial HCO3 immediately after exercise and during the first 8 h recovery. During recovery, lactate was retained in the white muscle at higher concentrations than in the plasma despite increased lactate efflux from the muscle. Pyruvate dehydrogenase activity was very low in dogfish white muscle at rest and during recovery (0.53±0.15 nmol g wet tissue−1 min−1; n=40) indicating that lactate oxidation is not the major fate of lactate during post-exercise recovery. The lack of change in white muscle free-carnitine and variable changes in short-chain fatty acyl-carnitine suggest that dogfish white muscle does not rely on lipid oxidation to fuel exhaustive exercise or recovery. These findings support the notion that extrahepatic tissues cannot utilize fatty acids as an oxidative fuel. Furthermore, our data strongly suggest that ketone body oxidation is important in fuelling recovery metabolism in dogfish white muscle and at least 20% of the ATP required for recovery could be supplied by uptake and oxidation of β-hydroxybutyrate from the plasma.

This is a preview of subscription content, access via your institution.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.



free coenzyme A


carnitine palmitoyltransferase-1


creatine phosphate

ΔH+ m :

metabolic proton load


lactate load


pyruvate dehydrogenase




short-chain fatty acyl-carnitine




trancutaneous electrical nerve stimulator


  • Ballantyne JS (1997) Jaws: the inside story. The metabolism of elasmobranch fishes. Comp Biochem Physiol B 118:703–742

    Article  Google Scholar 

  • Ballantyne JS, Glemet HC, Chamberlin ME, Singer TD (1993) Plasma nonesterified fatty acid of marine teleost and elasmobranch fishes. Mar Biol 116:47–52

    CAS  Google Scholar 

  • Bergmeyer H (1983) Methods of enzymatic analysis. Academic Press, New York

  • Boutilier RG, Heming TA, Iwama GK (1984) Appendix: physicochemical parameters for use in fish respiratory physiology. In: Hoar WS, Randall DJ (eds) Fish physiology, vol 10A. Academic Press, New York, pp 403–430

  • Cameron JN, Heisler N (1983) Studies of ammonia in rainbow trout: physico-chemical parameters, acid-base behaviour and respiratory clerance. J Exp Biol 105:107–125

    CAS  Google Scholar 

  • Cederblad G, Carlin JI, Constantin-Teodosiu D, Harper P, Hultman E (1990) Radioisotopic assays of CoASH and carnitine and their acetylated forms in human skeletal muscle. Anal Biochem 185:274–278

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Dobson GP, Hochachka PW (1987) Role of glycolysis in adenylate depletion and repletion during work and recovery in teleost white muscle. J Exp Biol 129:124–140

    Google Scholar 

  • Gilmour KM, Perry SF, Bernier NJ, Henry RP, Wood CM (2001) Extracellular carbonic anhydrase in the dogfish, Squalus acanthias: a role in CO2 excretion. Physiol Biochem Zool 74:477–492

    CAS  PubMed  Google Scholar 

  • Gilmour KM, Shah B, Szebedinszky C (2002) An investigation of carbonic anhydrase activity in the gills and blood plasma of brown bullhead (Ameiurus nebulosus), longnose skate (Raja rhina), and spotted ratfish (Hydrolagus colliei). J Comp Physiol B 172:77–86

    PubMed  Google Scholar 

  • Hassid W, Abraham S (1957) Chemical procedures for analysis of polysaccharides. In: Colowick S, Kaplan N (eds) Methods in enzymology, vol 3. Academic Press, New York

  • Heisler N, Neumann P, Holeton GF (1980) Mechanisms of acid-base adjustment in dogfish (Scyliorhinus stellaris) subjected to long-term temperature acclimation. J Exp Biol 85:99–110

    CAS  Google Scholar 

  • Holeton GF, 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

    CAS  PubMed  Google Scholar 

  • Kieffer JD (2000) Limits to exhaustive exercise in fish. Comp Biochem Physiol 126A:161–179

    CAS  Google Scholar 

  • Labree K, Milligan CL (1999) Lactate transport across sarcolemmal vesicles isolated from rainbow trout white muscle. J Exp Biol 202:2167–2175

    PubMed  Google Scholar 

  • Leech AR, Goldstein L, Cha C, Goldstein JM (1979) Alanine biosynthesis during starvation in skeletal muscle of the spiny dogfish, Squalus acanthias. J Exp Zool 207:73–80

    CAS  Google Scholar 

  • Milligan CL (1996) Metabolic recovery from exhaustive exercise in rainbow trout. Comp Biochem Physiol 113A:51–60

    Article  CAS  Google Scholar 

  • Milligan CL, Wood CM (1986) Tissue intracellular acid-base status and the fate of lactate after exhaustive exercise in the rainbow trout. J Exp Biol 123:123–144

    CAS  PubMed  Google Scholar 

  • Mommsen TP, Hochachka PW (1988) The purine nucleotide cycle as two temporally separated metabolic units: a study on trout muscle. Metabolism 37:552–556

    CAS  PubMed  Google Scholar 

  • Moyes CD, West TG (1995) Exercise metabolism of fish. In: Hochachka P, Mommsen T (eds) Molecular biology of fishes, vol 4. Elsevier, Amsterdam, pp 367–392

  • Moyes CD, Buck LT, Hochachka PW (1990) Mitochondrial and peroxisomal fatty acid oxidation in elasmobranchs. Am J Physiol 258:R756–R762

    CAS  PubMed  Google Scholar 

  • Moyes CD, Schulte PM, Hochachka PW (1992) Recovery metabolism of trout white muscle: role of mitochondria. Am J Physiol 262:R295–R304

    CAS  PubMed  Google Scholar 

  • Part P, Wright PA, Wood CM (1998) Urea and water permeability in dogfish (Squalus acanthias) gills. Comp Biochem Physiol A 119:117–123

    CAS  Google Scholar 

  • Piiper J, Meyer M, Drees F (1972) Hydrogen ion balance in the elasmobranch Scyliorhinus stellaris after exhausting activity. Respir Physiol 16:290–303

    Article  CAS  PubMed  Google Scholar 

  • Richards JG, Heigenhauser GJF, Wood CM (2002a) Glycogen phosphorylase and pyruvate dehydrogenase transformation in white muscle of trout during high-intensity exercise. Am J Physiol 282:R828–R836

    CAS  Google Scholar 

  • Richards JG, Heigenhauser GJF, Wood CM (2002b) Lipid oxidation fuels recovery from exhaustive exercise in white muscle of rainbow trout. Am J Physiol 282:R89–R99

    CAS  Google Scholar 

  • Schulte PM, Moyes CD, Hochachka PW (1992) Integrating metabolic pathways in post-exercise recovery of white muscle. J Exp Biol 166:181–195

    CAS  PubMed  Google Scholar 

  • Wang Y, Heigenhauser GJF, Wood CM (1994) Integrated responses to exhaustive exercise and recovery in rainbow trout white muscle: acid-base, phosphogen, carbohydrate, lipid, ammonia, fluid volume and electrolyte metabolism. J Exp Biol 195:227–258

    CAS  PubMed  Google Scholar 

  • Wang Y, Heigenhauser GJ, Wood CM (1996a) Ammonia movement and distribution after exercise across white muscle cell membranes in rainbow trout. Am J Physiol 271:R738–R750

    CAS  PubMed  Google Scholar 

  • Wang Y, Heigenhauser GJ, Wood CM (1996b) Lactate and metabolic H+ transport and distribution after exercise in rainbow trout white muscle. Am J Physiol 271:R1239–R1250

    CAS  PubMed  Google Scholar 

  • Wang Y, Wright PM, Heigenhauser GJF, Wood CM (1997) Lactate transport by rainbow trout white muscle: kinetic characteristics and sensitivity to inhibitors. Am J Physiol 272:R1577–R1587

    CAS  PubMed  Google Scholar 

  • Wang Y, Henry RP, Wright PM, Heigenhauser GJF, Wood CM (1998) Respiratory and metabolic functions of carbonic anhydrase in exercised white muscle of trout. Am J Physiol 275:R1766–R1779

    CAS  PubMed  Google Scholar 

  • Watson RR, Dickson KA (2001) Enzyme activities support the use of liver lipid-derived ketone bodies as aerobic fuels in muscle tissues of active sharks. Physiol Biochem Zool 74:273–282

    Article  CAS  PubMed  Google Scholar 

  • Wood CM, Perry SF (1985) Respiratory, circulatory, and metabolic adjustments to exercise in fish. In: Gilles R (ed) Circulation, respiration, metabolism. Springer, Berlin Heidelberg New York, pp 2–22

  • Wright PA, Randall DJ, Wood CM (1988) The distribution of ammonia and H+ ions between tissue compartments in lemon sole (Parophrys vetulus) at rest, during hypercapnia and following exercise. J Exp Biol 136:149–175

    CAS  Google Scholar 

  • Zammit VA, Newsholme EA (1979) Activities of enzymes of fat and ketone-body metabolism and effects of starvation on blood concentrations of glucose and fat fuels in teleost and elasmobranch fish. Biochem J 184:313–322

    CAS  PubMed  Google Scholar 

Download references


We gratefully acknowledge the technical assistance of Linda Diao and Nathan Webb and Bamfield Marine Station for their hospitality and infrastructure support. This work was supported by grants from the Natural Sciences and Engineering Research Council (NSERC) of Canada to C.M.W. and the Canadian Institutes of Health Research to G.J.F.H. An NSERC post-graduate scholarship and an Ontario Graduate Scholarship supported J.G.R. J.G.R. was awarded the Leo Margolis Scholarship from the Canadian Society of Zoologists to work at Bamfield. The Canada Research Chair Program supports C.M.W.

Author information

Authors and Affiliations


Corresponding author

Correspondence to J. G. Richards.

Additional information

Communicated by: L.C.-H. Wang

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Richards, J.G., Heigenhauser, G.J.F. & Wood, C.M. Exercise and recovery metabolism in the pacific spiny dogfish (Squalus acanthias). J Comp Physiol B 173, 463–474 (2003).

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:


  • Elasmobranch white muscle
  • β-Hydroxybutyrate
  • Lipid
  • Carbohydrate
  • Lactate