Journal of Comparative Physiology B

, Volume 160, Issue 6, pp 627–635 | Cite as

Fuel homeostasis in the harbor seal during submerged swimming

  • R. W. Davis
  • M. A. Castellini
  • T. M. Williams
  • G. L. Kooyman
Article

Summary

  1. 1.

    The turnover rates and oxidation rates of plasma glucose, lactate, and free fatty acids (FFA) were measured in three harbor seals (average mass=40 kg) at rest or during voluntary submerged swimming in a water flume at 35% (1.3 m·s-1) and 50% (2 m·s-1) of maximum oxygen consumption (MO2max).

     
  2. 2.

    For seals resting in water, the total turnover rates for glucose, lactate, and FFA were 23.2, 26.2, and 7.5 μmol·min-1·kg-1, respectively. Direct oxidation of these metabolites accounted for approximately 7%, 27%, and 33% of their turnover and 3%, 7%, and 18% of the total ATP production, respectively.

     
  3. 3.

    For swimming seals,MO2max was achieved at a drag load equivalent to a speed of 3 m·s-1 and averaged 1.85 mmol O2·min-1·kg-1, which is 9-fold greater than resting metabolism in water at 18°C.

     
  4. 4.

    At 35% and 50%MO2max, glucose turnover and oxidation rates did not change from resting levels. Glucose oxidation contributed about 1% of the total ATP production during swimming.

     
  5. 5.

    At 50%MO2max, lactate turnover and anaerobic ATP production doubled, but the steady state plasma lactate concentration remained low at 1.1 mM. Lactate oxidation increased 63% but still contributed only 4% of the total ATP production. Anaerobic metabolism contributed about 1% of the total ATP production at rest and during swimming.

     
  6. 6.

    The plasma FFA concentration and turnover rate inereased only 24% and 37% over resting levels, respectively, at 50%MO2max. However, the oxidation rate increased almost 3.5-fold and accounted for 85% of the turnover. The percentage of total ATP produced (21%) from FFA oxidation at 35% and 50%MO2max did not increase greatly over that at rest.

     
  7. 7.

    Dive duration decreased from 78 s while resting in water to 28 s at 50%MO2max.

     
  8. 8.

    The RQ ranged from 0.78 at rest to 0.74 at 50%MO2max, indicating that fat was an important source of energy during submerged swimming.

     
  9. 9.

    By adjusting breath-hold duration during strenuous underwater swimming, harbor seals are able to maintain an aerobic, fat-based metabolism.

     

Key words

Phoca vitulina Swimming Metabolism Fuel 

Abbreviations

ATP

adenosine-triphosphate

[LAC]

lactate concentration

[GLU]

glucose concentration

[FFA]

free fatty acid concentration

MO2

oxygen consumption

MO2max

maximum oxygen consumption

MCO2

carbon dioxid production

RQ

respiratory quotient

TG

triglycerides

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Bergmann SR, Carlson E, Dannen E, Sabel BE (1980) An improved assay with 4-(2-thiazolylazo)-resorcinol for non-esterified fatty acids in biological fluids. Clin Chem Acta 107:53–63Google Scholar
  2. Blazquez E, Castro M, Herrera E (1971) Effect of high-fat diet on pancreatic insulin release, glucose tolerance and hepatic gluconeogenesis in male rats. Rev Espan Fisol 27:297–304Google Scholar
  3. Castellini MA (1988) Visualizing metabolic transitions in aquatic mammals: does apnea plus swimming equal “diving”? Can J Zool 66:40–44Google Scholar
  4. Castellini MA, Murphy BJ, Fedak M, Ronald K, Gofton H, Hochachka PW (1985) Potentially conflicting metabolic demands of diving and exercise in seals. J Appl Physiol 58(2):392–399Google Scholar
  5. Castellini MA, Costa DP, Huntley AC (1987) Fatty acid metabolism in fasting elephant seal pups. J Comp Physiol 3:445–449Google Scholar
  6. Castellini MA, Davis RW, Kooyman GL (1988) Blood chemistry regulation during repetitive diving in Weddell seals. Physiol Zool 61(5):379–386Google Scholar
  7. Davis RW (1983) Lactate and glucose metabolism in the resting and diving harbor seal (Phoca vitulina) J Comp Physiol 153:275–288Google Scholar
  8. Davis RW, Williams TW, Kooyman GL (1985) Swimming metabolism of yearling and adult harbor sealsPhoca vitulina. Physiol Zool 58(5):590–596Google Scholar
  9. Depocas F, DeFreitas ASW (1970) Method for estimating rates of formation and interconversion of glucose-glycerol and glucoselactic acid in intact animals. Can J Physiol Pharmacol 48:557–560Google Scholar
  10. Elsner R, Gooden B (1983) Diving and asphyxia: A comparative study of animals and man. Cambridge University Press, CambridgeGoogle Scholar
  11. Elsner R (1986) Limits to exercise performance: some ideas from comparative studies. Acta Physiol Scand 128(Suppl 556):45–51Google Scholar
  12. Fedak MA, Pullen MR, Kanwisher J (1988) Circulatory responses of seals to periodic breathing: heart rate and breathing during exercise and diving in the laboratory and open sea. Can J Zool 66:53–60Google Scholar
  13. George JC, Vallyathan NV, Ronald K (1971) The harp seal,Pagophilus groenlandicus (Erxleben, 1777). VII. A histophysiological study of certain skeletal muscles. Can J Zool 49:25–30Google Scholar
  14. Guppy M, Hill RD, Schneider RC, Qvist J, Liggins GC, Zapol WM, Hochachka PW (1986) Microcomputer-assisted metabolic studies of voluntary diving of Weddell seals. Am J Physiol 250:R175–R187Google Scholar
  15. Havel RJ, Carlson LA (1963) Comparative turnover rates of free fatty acids and glycerol in blood of dogs under various conditions. pp 651–658 in Life Sciences No. 9. Pergamon New YorkGoogle Scholar
  16. Havel RJ, Carlson, LA, Eklund, LG, Holmgren, A (1964) Turnover rate and oxidation of different free fatty acids in man during exercise. J Appl Physiol 19:613–618Google Scholar
  17. Issekutz B Jr, Miller HI, Paul P, Rodahl K (1964) Source of fat oxidation in exercising dogs. Am J Physiol 207(3):583–58Google Scholar
  18. Issekutz B Jr, Paul P, Miller HI (1967) Metabolism in normal and pancreatectomized dogs during steady-state exercise. Am J PHysiol 213:857–862Google Scholar
  19. Issekutz B Jr, Paul P (1968) Intramuscular energy sources in exercising and pancreatectomized dogs. Am J Physiol 215:197–204Google Scholar
  20. Jangaard PM, Ackman RG, Burgher RD (1963) Component fatty acids of the blubber fat from the common or harbor sealPhoca vitulina concolor De Kay. Can J Biochem Physiol 41:2543–2546Google Scholar
  21. Jones GB (1965) Determination of specific activity of labeled blood glucose by liquid scintillation using glucose pentaacetate. Anal Biochem 12:249–258Google Scholar
  22. Jones DR, Fisher D, McTaggart S, West NH (1973) Heart rate during breath-holding and diving in the unrestrained harbor seal (Phoca vitulina richardi). Can J Zool 51:671–680Google Scholar
  23. Kettelhut IC, Foss MC, Migliorini RH (1980) Glucose homeostasis in a carnivorous animal (cat) and in rats fed a high-protein diet. Am J Physiol 239:R437–R444Google Scholar
  24. Kooyman GL, Campbell WB (1972) Heart rates in freely diving Weddell seals,Leptonychotes weddellii. Comp Biochem Physiol [A] 43:31–36Google Scholar
  25. Kooyman GL, Wahrenbrock EA, Castellini MA, Davis RW, Sinnett EE (1980) Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J Comp Physiol 138:335–346Google Scholar
  26. Malmendier CL, Delcroix C, Berman M (1974) Interrelations in the oxidative metabolism of free fatty acids, glucose, and glycerol in normal and hyperlipemic patients. J Clin Invest 54(2):461–476Google Scholar
  27. Mazzeo RS, Brooks GA, Schoeller DA, Budinger TF (1986) Disposal of blood (1-13C) lactate in humans during rest and exercise. J Appl Physiol 60:232–241Google Scholar
  28. Neptune EM Jr., Sudduth HC, Foreman DR (1969) Labile fatty acids of rat diaphragm muscle and their possible role as the major endogenous substrate for maintenance of respiration. J Biol Chem 234(7):1659–1660Google Scholar
  29. Oscai LB, Caruso RA, Wergeles AC (1982) Lipoprotein lipase hydrolyzes endogenous triacylglycerols in muscle of exercised rats. J Appl Physiol: Respirat Environ Exercise Physiol 52(4):1059–1063Google Scholar
  30. Puppione DL, Nichols AV (1970) Characterization of the chemical and physical properties of the serum lipoproteins of certain marine mammals. Physiol Chem Phys 2:49–58Google Scholar
  31. Roberts S, Samuels LT, Reinecke RM (1943) Previous diet and the apparent utilization of fat in the absence of the liver. Am J Physiol 140:639–644Google Scholar
  32. Reilly PEB (1975) Use of reverse isotope dilution analysis to determine blood plasma (l-(+)-14C-lactate specific radioactivity. Anal Biochem 64:37–44Google Scholar
  33. Schmidt-Nielsen K (1975) Animal physiology: Adaptation and environment. Cambridge University Press, CambridgeGoogle Scholar
  34. Shimizu S, Inoue K, Tani Y, Yamada H (1979) Enzymatic determination of serum free fatty acids. Anal Biochem 98:341–345Google Scholar
  35. Steele R, Wall JS, De Bodo RC, Altzuler N (1956) Carbohydrate metabolism of hypophysectomized dogs as studied with radioactive glucose. Am J Physiol 1187:25–31Google Scholar
  36. Taylor CR, Karas RH, Weibel ER, Hoppler H (1987) Adaptive variation in the mammalian respiratory system in relation to energetic demand. II. Reaching the limits of oxygen flow. Respir Physiol 67:7–26Google Scholar
  37. Williams TM, Kooyman GL (1990) The effects of exercise load on physiological responses of swimming seals and sea lions. J Comp Physiol 160:637–644Google Scholar
  38. Williams TM, Kooyman GL (1985) Swimming performance and hydrodynamic characteristics of harbor sealsPhoca vitulina. Physiol Zool 58(5):576–589Google Scholar
  39. Wolfe RR, Burke J (1977) Effect of burn trauma on glucose turnover, oxidation, and recycling in guinea pigs. Am J Physiol 233:E80–E85Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • R. W. Davis
    • 1
  • M. A. Castellini
    • 2
  • T. M. Williams
    • 3
  • G. L. Kooyman
    • 1
  1. 1.Physiological Research LaboratoryScripps Institution of OceanographyLa JollaUSA
  2. 2.Institute of Marine ScienceUniversity of AlaskaFairbanksUSA
  3. 3.Naval Oceans Systems CenterKailuaUSA

Personalised recommendations