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Metabolic responses to exhaustive exercise change markedly during the protracted non-trophic spawning migration of the lamprey Geotria australis

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Abstract

Adults of the Southern hemisphere lamprey Geotria australis were subjected to an exercise/recovery regime at the commencement and end of their 12–15 month non-trophic, upstream spawning migration. In early (immature) migrants and pre-spawning females, muscle glycogen was markedly depleted during exercise, but became rapidly replenished. As muscle lactate rose during exercise and peaked 1–1.5 h into the recovery period, and therefore after muscle glycogen had become replenished, it cannot be the direct source for that replenishment. However, both plasma lactate and glycerol (but not muscle glycerol and glucose) rose sharply during exercise and then declined markedly during the first 0.5 h of recovery and thus exhibited the opposite trend to that of muscle glycogen, implying that these limited pools of glycogenic precursors contribute to glycogen replenishment. Although plasma glucose rose following exercise, and consequently could also be a precursor for muscle glycogen replenishment, it remained elevated even after muscle glycogen had become replenished. While resting pre-spawning females and mature males retained high muscle glycogen concentrations, this energy store became permanently depleted in females during spawning. In mature males, muscle glycogen remained high and lactate low during the exercise/recovery regime, whereas muscle glycerol declined precipitously during exercise and then rose rapidly. In summary, vigorous activity by G. australis is fuelled extensively by anaerobic metabolism of glycogen early in the spawning run and by pre-spawning females, but by aerobic metabolism of its energy reserves in mature males.

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References

  • Beamish FWH, Potter IC, Thomas E (1979) Proximate composition of the adult anadromous sea lamprey Petromyzon marinus, in relation to feeding migration and reproduction. J Anim Ecol 48:1–19

    Article  Google Scholar 

  • Bergmeyer HU (1974) Methods of enzymatic analysis. Academic Press, New York

    Google Scholar 

  • Bergmeyer HU (1983) Metabolites I. Carbohydrates. Methods of enzymatic analysis. Academic Press, New York

    Google Scholar 

  • Bird DJ, Potter IC (1983a) Changes in the fatty acid composition of triacylglycerols and phospholipids during the life cycle of the lamprey Geotria australis Gray. Comp Biochem Physiol Part B Biochem Mol Biol 75B:31–41

    Article  CAS  Google Scholar 

  • Bird DJ, Potter IC (1983b) Proximate composition at various stages of adult life in the southern hemisphere lamprey Geotria australis Gray. Comp Biochem Physiol Part A Physiol 74A:623–633

    Article  Google Scholar 

  • Bird DJ, Lutz PL, Potter IC (1976) Oxygen dissociation curves of the blood of larval and adult lampreys (Lampetra fluviatilis). J Exp Biol 65:449–458

    PubMed  CAS  Google Scholar 

  • Boutilier RG, Ferguson RA, Henry RP, Tufts BL (1993) Exhaustive exercise in the sea lamprey (Petromyzon marinus): relationship between anaerobic metabolism and intracellular acid–base balance. J Exp Biol 178:71–88

    CAS  Google Scholar 

  • Cake MH, Power GW, Potter IC (1995) The liver and muscle of early upstream migrant lampreys (Geotria australis) contain high levels of acetyl-CoA carboxylase and a carnitine palmitoyl transferase I that is sensitive to malonyl-CoA. Comp Biochem Physiol Part B Biochem Mol Biol 110:417–423

    Article  Google Scholar 

  • Emelyanova LV, Koroleva EM, Savina MV (2004) Glucose and free amino acids in the blood of lampreys (Lampetra fluviatilis L.) and frogs (Rana temporaria L.) under prolonged starvation. Comp Biochem Physiol Part A 138:527–532

    Article  Google Scholar 

  • European Medicines Agency (2002) Report of the committee for veterinary medicinal products—benzocaine (extension to Salmonidae). pp 1–5

  • Fellows FCI, McLean RM (1982) A study of the plasma lipoproteins and the tissue lipids of the migrating lamprey, Mordacia mordax. Lipids 17:741–747

    Article  PubMed  CAS  Google Scholar 

  • Gardner GE, Kennedy L, Milton JTB, Pethick DW (1999) Glycogen metabolism and ultimate pH of muscle in Merino, first-cross and second-cross wether lambs as affected by stress before slaughter. Aust J Agric Res 50:175–181

    Article  CAS  Google Scholar 

  • Hardisty MW (2006) Lampreys. Life without jaws. Forest Text, Ceredigion, Wales

    Google Scholar 

  • Hardisty MW, Potter IC (1971a) The behaviour ecology and growth of larval lampreys. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 1. Academic Press, London, pp 85–125

    Google Scholar 

  • Hardisty MW, Potter IC (1971b) The general biology of adult lampreys. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 1. Academic Press, London, pp 127–206

    Google Scholar 

  • Hardisty MW, Rovainen CM (1982) Morphology and functional aspects of the muscular system. In: Hardisty MW, Potter IC (eds) The biology of lampreys, vol 4A. Academic Press, London, pp 137–231

    Google Scholar 

  • Hassid WZ, Abraham S (1957) Chemical procedures for analysis of polysaccharides. In: Colowick SP, Kaplan NO (eds) Methods in enzymology. Academic Press, New York, pp 34–39

    Chapter  Google Scholar 

  • Hochachka PW, Mommsen TP (1983) Protons and anaerobiosis. Science 219:1391–1397

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kieffer JD, Tufts BL (1996) The influence of environmental temperature on the role of the rainbow trout gill in correcting the acid–base disturbance following exhaustive exercise. Physiol Zool 69:1301–1323

    Google Scholar 

  • Mesa MG, Bayer JM, Seelye JG (2003) Swimming performance and physiological responses to exhaustive exercise in radio-tagged and untagged pacific lampreys. Trans Am Fish Soc 132:483–492

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Milligan CL, Girard SS (1993) Lactate metabolism in rainbow trout. J Exp Biol 180:175–193

    CAS  Google Scholar 

  • Milligan CL, Wood CM (1986a) 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

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Milligan CL, Hooke GB, Johnson C (2000) Sustained swimming at low velocity following a bout of exhaustive exercise enhances metabolic recovery in rainbow trout. J Exp Biol 203:921–926

    PubMed  CAS  Google Scholar 

  • Moore JW, Mallatt JM (1980) Feeding of larval lamprey. Can J Fish Aquat Sci 37:1658–1664

    Article  Google Scholar 

  • Morris R (1980) Blood composition and osmoregulation in ammocoete larvae. Can J Fish Aquat Sci 37:1665–1679

    Article  CAS  Google Scholar 

  • Paton KR, Cake MH, Potter IC (2001) Muscle glycogen, lactate and glycerol-3-phosphate concentrations of larval and young adult lampreys in response to exercise. Comp Biochem Physiol Part B 129:759–766

    Article  CAS  Google Scholar 

  • Pearson MP, Spriet LL, Stevens ED (1990) Effect of sprint training on swim performance and white muscle metabolism during exercise and recovery in rainbow trout (Salmo gairdneri). J Exp Biol 149:45–60

    Google Scholar 

  • Plisetskaya E (1980) Fatty acid levels in blood of cyclostomes and fish. Environ Biol Fish 5:273–290

    Article  CAS  Google Scholar 

  • Potter IC (1980) Ecology of larval and metamorphosing lampreys. Can J Fish Aquat Sci 37:1641–1657

    Article  Google Scholar 

  • Potter IC, Beamish FWH (1977) The freshwater biology of adult anadromous sea lampreys Petromyzon marinus. J Zool Lond 181:113–130

    Article  Google Scholar 

  • Potter IC, Hilliard RW (1986) Growth and the average duration of larval life in the southern hemisphere lamprey Geotria australis Gray. Experientia 42:1170–1173

    Article  Google Scholar 

  • Potter IC, Strahan R (1968) The taxonomy of the lampreys Geotria and Mordacia and their distribution in Australia. Proc Linn Soc Lond 179:229–240

    Article  Google Scholar 

  • Potter IC, Hill BJ, Gentleman S (1970) Survival and behaviour of ammocoetes at low oxygen tensions. J Exp Biol 53:59–73

    PubMed  CAS  Google Scholar 

  • Potter IC, Hilliard RW, Bird DJ, Macey DJ (1983) Quantitative data on morphology and organ weights during the protracted spawning-run period of the Southern Hemisphere lamprey Geotria australis. J Zool Lond 200:1–20

    Article  Google Scholar 

  • Renaud CB, Gill HS, Potter IC (2009) Relationships between the diets and characteristics of the dentition, buccal glands and velar tentacles of the adults of the parasitic species of lampreys. J Zool Lond 278:231–242

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ross LG, Ross B (2008) Anaesthetic and sedative techniques for aquatic animals. Blackwell, Oxford, UK

    Book  Google Scholar 

  • Savina MV, Wojtczak AB (1977) Enzymes of gluconeogenesis and the synthesis of glycogen from glycerol in various organs of the lamprey (Lampetra fluviatilis). Comp Biochem Physiol Part B Biochem Mol Biol 57B:185–190

    Article  Google Scholar 

  • Sugita T, Shimeno S, Nakono N, Hosokawa H, Masumoto T (2001) Response of enzyme activities and metabolic intermediate concentrations to a long burst of exercise and following resting in muscle and the hepatopancreas of carp. Fish Sci 67:904–911

    Article  CAS  Google Scholar 

  • Thorson TB (1959) Partitioning of body water in sea lamprey. Science 130:99–100

    Article  PubMed  CAS  Google Scholar 

  • Tufts BL (1991) Acid–base regulation and blood gas transport following exhaustive exercise in an agnathan, the sea lamprey Petromyzon marinus. J Exp Biol 159:371–385

    PubMed  CAS  Google Scholar 

  • Van Ginneken V, Coldenhoff K, Boot R, Hollander J, Lefeber F, Van den Thillart G (2008) Depletion of high energy phosphates implicates post-exercise mortality in carp and trout; an in vivo 31P-NMR study. Comp Biochem Physiol 149A:98–108

    Google Scholar 

  • Wang Y, Wright P (1997) Lactate transport by rainbow trout white muscle: kinetic characteristics and sensitivity to inhibitors. Am J Physiol Regul Integr Comp Physiol 41:R1577–R1587

    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

    PubMed  CAS  Google Scholar 

  • Wieland O (1974) Glycerol UV-method. In: Bergmeyer HU (ed) Methods in enzymatic analysis. Academic Press, New York, pp 1404–1408

    Google Scholar 

  • Wilkie MP, Couturier J, Tufts BL (1998) Mechanisms of acid–base regulation in migrant sea lampreys (Petromyzon marinus) following exhaustive exercise. J Exp Biol 201:1473–1482

    PubMed  CAS  Google Scholar 

  • Wilkie MP, Bradshaw PG, Joanis V, Claude JF, Swindell SL (2001) Rapid metabolic recovery following vigorous exercise in burrow-dwelling larval sea lampreys (Petromyzon marinus). Physiol Biochem Zool 74:261–283

    Article  PubMed  CAS  Google Scholar 

  • Wilkie MP, Claude JF, Cockshutt A, Holmes JA, Wang YS, Youson JH, Walsh PJ (2006) Shifting patterns of nitrogen excretion and amino acid catabolism capacity during the life cycle of the sea lamprey (Petromyzon marinus). Physiol Biochem Zool 79:885–898

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Wood CM, McMahon BR, McDonald DG (1977) An analysis of changes in blood pH following exhausting activity in the starry flounder, Platichthys stellatus. J Exp Biol 69:173–185

    PubMed  CAS  Google Scholar 

  • Youson JH (1980) Morphology and physiology of lamprey metamorphosis. Can J Fish Aquat Sci 37:1687–1710

    Article  Google Scholar 

Download references

Acknowledgments

David Morgan, Howard Gill and David Macey are thanked for their invaluable assistance in collecting or maintaining lampreys. Particular gratitude is expressed to the two anonymous referees, whose constructive criticisms led to us describing further data, modifying some of the implications of our results and producing a far more refined text. Financial support was provided by Murdoch University. Murdoch University Animal Ethics Committee, under Permit Number 799R, approved the experiments described in this paper.

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Correspondence to M. H. Cake.

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Communicated by I.D. Hume.

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Paton, K.R., Cake, M.H. & Potter, I.C. Metabolic responses to exhaustive exercise change markedly during the protracted non-trophic spawning migration of the lamprey Geotria australis . J Comp Physiol B 181, 751–763 (2011). https://doi.org/10.1007/s00360-011-0570-6

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