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

Abstract

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.

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Abbreviations

CoA-SH:

free coenzyme A

CPT-1:

carnitine palmitoyltransferase-1

CrP:

creatine phosphate

ΔH+ m :

metabolic proton load

ΔLac:

lactate load

PDH:

pyruvate dehydrogenase

PVP:

polyvinylpyrrolidone

SCFA-carnitine:

short-chain fatty acyl-carnitine

TAG:

triacylglycerol

TENS:

trancutaneous electrical nerve stimulator

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Acknowledgements

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.

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Correspondence to J. G. Richards.

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Communicated by: L.C.-H. Wang

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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). https://doi.org/10.1007/s00360-003-0354-8

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Keywords

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