Advertisement

Development of myoglobin concentration and acid buffering capacity in harp (Pagophilus groenlandicus) and hooded (Cystophora cristata) seals from birth to maturity

  • Keri C. LestykEmail author
  • L. P. Folkow
  • A. S. Blix
  • M. O. Hammill
  • J. M. Burns
Original Paper

Abstract

Pinnipeds rely on muscle oxygen stores to help support aerobic diving, therefore muscle maturation may influence the behavioral ecology of young pinnipeds. To investigate the pattern of muscle development, myoglobin concentration ([Mb]) and acid buffering ability (β) was measured in ten muscles from 23 harp and 40 hooded seals of various ages. Adult [Mb] ranged from 28–97 to 35–104 mg g tissue−1 in harp and hooded seals, respectively, with values increasing from the cervical, non-swimming muscles to the main swimming muscles of the lumbar region. Neonatal and weaned pup muscles exhibited lower (~30% adult values) and less variable [Mb] across the body than adults. In contrast, adult β showed little regional variation (60–90 slykes), while high pup values (~75% adult values) indicate significant in utero development. These findings suggest that intra-uterine conditions are sufficiently hypoxic to stimulate prenatal β development, but that [Mb] development requires additional postnatal signal such as exercise, and/or growth factors. However, because of limited development in both β and [Mb] during the nursing period, pups are weaned with muscles with lower aerobic and anaerobic capacities than those of adults.

Keywords

Myoglobin Acid buffering Muscle development Harp seal Hooded seal 

Abbreviations

β

Acid buffering capacity, slykes

βTBA

Total body acid buffering capacity

βLD

Acid buffering capacity for the longissimus dorsi

βPEC

Acid buffering capacity for the pectoralis

LD

Longissimus dorsi

Mb

Muscle myoglobin, mg g wet tissue−1

[Mb]TBA

Total body myoglobin concentration

[Mb]LD

Myoglobin concentration for the longissimus dorsi

[Mb]PEC

Myoglobin concentration for the pectoralis

Pec

Pectoralis

PWF

Postweaning fast

Notes

Acknowledgments

We thank the Captain and crew of R/V Jan Mayen, and Mrs. Monica Jenstad for their assistance in the field in Norway. In Canada, we thank the Canadian Coast Guard helicopter pilots Harrison McRae and Bruce Kendall, the Château Madelinot and Roger Simon for providing laboratory space, and Dr. Lena Measures, Stephan Pillet, and Sam Turgeon for assistance with sample processing and analysis. Animal capture and experimental protocols were conducted under permit from the Royal Norwegian Ministry of Fisheries, the Norwegian National Animal Research Authority (NARA), the University of California Chancellor’s Committee on Animal Research, the Department of Fisheries and Oceans, Canada and the University of Alaska Anchorage Institutional Animal Care and Use Permits. All samples were imported into the United States under Marine Mammal permits 782-1399 and 782-1694-02. This study was financed in part by contributions from Alaska EPSCoR (NSF EPS-0346770), the Institute of Marine Science, University of California Santa Cruz, the Roald Amundsen Center for Arctic Research, University of Tromsø, and the Department of Fisheries and Oceans, Canada.

References

  1. Bajzak, CE, Côté SD, Hammill MO, Stenson G (2009) Intersexual differences in the postbreeding behaviour of the Northwest Atlantic hooded seal. Mar Ecol Prog Ser (in press)Google Scholar
  2. Baldwin KM, Haddad F (2001) Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle. J Appl Physiol 90:345–357CrossRefPubMedGoogle Scholar
  3. Bangsbo J, Madsen K, Kiens B, Richter EA (1996) Effect of muscle acidity on muscle metabolism and fatigue during intense exercise in man. J Physiol 495:587–596PubMedGoogle Scholar
  4. Bate Smith EC (1938) The buffering of muscle in rigor: protein, phosphate and carnosine. J Physiol 92:336–343Google Scholar
  5. Blix AS, Steen JB (1979) Temperature regulation in newborn polar homeotherms. Physiol Rev 59:285–304PubMedGoogle Scholar
  6. Bodkin JL, Esslinger GJ, Monson DH (2004) Foraging depths of sea otters and implications to costal marine communities. Mar Mamm Sci 20:305–321CrossRefGoogle Scholar
  7. Bowen WD, Boness DJ, Oftedal OT (1987) Mass transfer from mother to pup and subsequent mass loss by the weaned pup in the hooded seal, Cystophora cristata. Can J Zool 65:1–8CrossRefGoogle Scholar
  8. Bowen WD, Boness DJ, Iverson SJ (1999) Diving behaviour of lactating harbour seals and their pups during maternal foraging trips. Can J Zool 77:978–988CrossRefGoogle Scholar
  9. Brooks GA, Fahey TD, Baldwin KM (2005) Exercise physiology, 4th edn. McGraw-Hill, New YorkGoogle Scholar
  10. Bryden MM (1972) Body size and composition of elephant seals Mirounga leonina: absolute measurements and estimates from bone dimensions. J Zool Lond 167:265–276CrossRefGoogle Scholar
  11. Burns JM, Costa DP, Frost KJ, Harvey JT (2005) Physiological development in juvenile harbor seals. Phys Bioch Zool 78:1057–1068CrossRefGoogle Scholar
  12. Burns JM, Lestyk K, Folkow LP, Hammill MO, Blix AS (2007) Size and distribution of oxygen stores in harp and hooded seals from birth to maturity. J Comp Physiol B 177:687–700CrossRefPubMedGoogle Scholar
  13. Burton RF (1978) Intracellular buffering. Respir Physiol 33:51–58CrossRefPubMedGoogle Scholar
  14. Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–899PubMedGoogle Scholar
  15. Carrier DR (1983) Postnatal ontogeny of the musculo-skeletal system in the black-tailed jack rabbit (Lepus californicus). J Zool 201:27–55CrossRefGoogle Scholar
  16. Castellini MA, Somero GN (1981) Buffering capacity of vertebrate muscle: correlations with potential for anaerobic function. J Comp Physiol 143:191–198Google Scholar
  17. Clark CA, Burns JM, Schreer JF, Hammill MO (2007) A longitudinal and cross-sectional analysis of total body oxygen store development in nursing harbor seals (Phoca vitulina). J Comp Physiol B 177:217–227CrossRefPubMedGoogle Scholar
  18. Close RI (1972) Dynamic properties of mammalian skeletal muscles. Physiol Rev 52:129–197PubMedGoogle Scholar
  19. Davis RW, Polasek L, Watson R, Fuson A, Williams TM, Kanatous SB (2004) The diving paradox: new insights into the role of the dive response in air-breathing vertebrates. Comp Biochem Physiol A 138:263–268CrossRefGoogle Scholar
  20. Evans BK, Jones DR, Baldwin J, Gabbott GRJ (1994) Diving ability of the platypus. Aust J Zool 42:17–27CrossRefGoogle Scholar
  21. Fish FE, Ronald SI (1988) Kinematics and estimated thrust production of swimming harp and ringed seals. J Exp Biol 137:157–173PubMedGoogle Scholar
  22. Folkow LP, Blix AS (1999) Diving behaviour of hooded seals (Cystophora cristata) in the Greenland and Norwegian Seas. Polar Biol 22:61–74CrossRefGoogle Scholar
  23. Folkow LP, Nordoy ES, Blix AS (2004) Distribution and diving behavior of harp seals (Pagophilus groenlandica) from the Greenland Sea stock. Polar Biol 27:281–298CrossRefGoogle Scholar
  24. Garry DJ, Bassel-Dubay R, Richarson JG, Neufer PD, Williams RS (1996) Postnatal development and plasticity of specialized fiber characteristics in the hindlimb. Dev Gen 19:146–156CrossRefGoogle Scholar
  25. George JC, Ronald K (1975) Metabolic adaptation in pinniped skeletal muscle. Rapp P -v Reun Cons int Explor Mer 169:432–436Google Scholar
  26. Grand TI (1977) Body weight: its relation to tissue composition, segment distribution, and motor function. Am J Phys Anthrop 47:211–240CrossRefPubMedGoogle Scholar
  27. Grand TI, Barboza PS (2001) Anatomy and development of the koala, Phascolarctos cinereus: an evolutionary perspective on the superfamily Vombatoidea. Anat Embryol 203:211–223CrossRefPubMedGoogle Scholar
  28. Greaves DK, Schreer JF, Hammill MO, Burns JM (2005) Diving heart rate development in postnatal harbour seals, Phoca vitulina. Phys Bioch Zool 78:9–17CrossRefGoogle Scholar
  29. Hochachka PW, Foreman RA (1993) Phocid and cetacean blueprints of muscle metabolism. Can J Zool 71:2089–2098CrossRefGoogle Scholar
  30. Holloszy JO, Booth FW (1976) Biochemical adaptations to endurance exercise in muscle. Ann Rev Physiol 38:273–291CrossRefGoogle Scholar
  31. Howell AB (1929) Anatomy of the eared and earless seals. Proc U S Natl Mus 73:1–142Google Scholar
  32. Jamon M (2006) The early development of motor control in neonate rat. Evol 5:657–666Google Scholar
  33. Jorgensen C, Lydersen C, Kovacs KM (2001) Diving development in nursing harbour seal pups. J Exp Biol 204:3993–4004PubMedGoogle Scholar
  34. Kanatous SB, DiMichele LV, Cowan DF, Davis RW (1999) High aerobic capacities in skeletal muscles of pinnipeds: adaptations to diving hypoxia. J Appl Physiol 86:1247–1256PubMedGoogle Scholar
  35. Kanatous SB, Davis RW, Watson R, Polasek L, Williams TM, Mathieu-Costello O (2002) Aerobic capacities in the skeletal muscles of Weddell seals: key to longer dive durations? J Exp Biol 205:3601–3608PubMedGoogle Scholar
  36. Kanatous SB, Hawke TJ, Trumble SJ, Pearson LP, Watson RR, Garry DJ, Williams TM, Davis RW (2008) The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals. J Exp Biol 211:2559–2565Google Scholar
  37. Kooyman GL (1989) Diverse divers: physiology and behavior. Springer, BerlinGoogle Scholar
  38. Kooyman GL, Castellini MA, Davis RW (1981) Physiology of diving in marine mammals. Ann Rev Physiol 43:343–356CrossRefGoogle Scholar
  39. Kooyman GL, Cherel Y, Le Maho Y, Croxall JP, Thorson P, Ridoux V, Kooyman CA (1992) Diving behavior and energetics during foraging cycles in king penguins. Ecol Monog 62:143–163CrossRefGoogle Scholar
  40. Kovacs KM, Lavigne DM (1986) Maternal investment and neonatal growth in phocid seals. J Anim Ecol 55:1035–1051CrossRefGoogle Scholar
  41. Kristensen M, Albertsen J, Rentsch M, Juel C (2005) Lactate and force production in skeletal muscle. J Physiol 562:521–526CrossRefPubMedGoogle Scholar
  42. Lenfant C, Johansen K, Torrance JD (1970) Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir Physiol 9:277–286CrossRefPubMedGoogle Scholar
  43. Liggins GC, Qvist J, Hochachka PW, Murphy BJ, Creasy RK, Schneider RC, Snider MT, Zapol WM (1980) Fetal cardiovascular and metabolic responses to simulated diving in the Weddell seal. J Appl Physiol 49:424–430PubMedGoogle Scholar
  44. Lydersen C, Ryg MS, Hammill MO, O’Brien J (1992) Oxygen stores and aerobic dive limit of ringed seals (Phoca hispida). Can J Zool 70:458–461CrossRefGoogle Scholar
  45. Lydersen C, Kovacs KM, Hammill MO (1997) Energetics during nursing and early postweaning fasting in hooded seal (Cystophora cristata) pups from the Gulf of St. Lawrence. J Comp Physiol B 167:81–88CrossRefPubMedGoogle Scholar
  46. MacArthur RA, Humphries MM, Fines GA, Campbell KL (2001) Body oxygen stores, aerobic dive limits, and the diving abilities of juvenile and adult muskrats (Ondatra zibethicus). Phys Bioch Zool 74:178–190CrossRefGoogle Scholar
  47. Merrick RL, Loughlin TR (1997) Foraging behavior of adult female and young-of-the-year Steller sea lions in Alaskan waters. Can J Zool 75:776–786CrossRefGoogle Scholar
  48. Muir GD (2000) Early ontogeny of locomotor behavior: a comparison between altricial and precocial animals. Brain Res Bull 53:719–726CrossRefPubMedGoogle Scholar
  49. Nordoy ES, Folkow LP, Potelov V, Prischemikhin V, Blix AS (2008) Seasonal distribution and dive behaviour of harp seals (Pagophilus groenlandicus) of the White Sea-Barents Sea stock. Polar Biol 31:1119–1135CrossRefGoogle Scholar
  50. Noren SR (2004) Buffering capacity of the locomotor muscle in cetaceans: correlates with postpartum development, dive duration, and swim performance. Mar Mamm Sci 20:808–822CrossRefGoogle Scholar
  51. Noren SR, Williams TM (2000) Body size and skeletal muscle myoglobin of cetaceans: adaptations for maximizing dive duration. Comp Biochem Physiol A 126:181–191CrossRefGoogle Scholar
  52. Noren SR, Williams TM, Pabst DA, McLellan WA, Dearolf JL (2001) The development of diving in marine endotherms: preparing the skeletal muscles of dolphins, penguins, and seals for activity during submergence. J Comp Physiol B 171:127–134CrossRefPubMedGoogle Scholar
  53. Noren SR, Iverson SJ, Boness DJ (2005) Development of the blood and muscle oxygen stores in gray seals (Halichoerus grypus): implications for juvenile diving capacity and the necessity of a terrestrial postweaning fast. Phys Bioch Zool 78:482–490CrossRefGoogle Scholar
  54. Oftedal OT, Bowen WD, Boness DJ (1996) Lactation performance and nutrient deposition in pups of the harp seal, Phoca groenlandica, on ice floes off southeast labrador. Physiol Zool 69:635–657Google Scholar
  55. Ontell M, Dunn RF (1978) Neonatal muscle growth: a quantitative study. Am J Anat 152:539–555CrossRefPubMedGoogle Scholar
  56. Peronnet F, Aguilaniu B (2006) Lactic acid buffering, nonmetabolic CO2 and exercise hyperventilation: A critical reappraisal. Respir Physiol Neurobiol 150:4–18CrossRefPubMedGoogle Scholar
  57. Pette D, Staron RS (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 116:1–76PubMedGoogle Scholar
  58. Picard B, Lefaucheur L, Berri C, Duclos MJ (2002) Muscle fibre ontogenesis in farm animal species. Reprod Nutr Dev 42:415–431CrossRefPubMedGoogle Scholar
  59. Ponganis PJ, Costello ML, Starke LN, Mathieu-Costello O, Kooyman GL (1997) Structural and biochemical characteristics of locomotory muscles of emperor penguins, Aptenodytes forsteri. Respir Physiol 109:73–80CrossRefPubMedGoogle Scholar
  60. Ponganis PJ, Starke LN, Horning M, Kooyman GL (1999) Development of diving capacity in emperor penguins. J Exp Biol 202:781–786PubMedGoogle Scholar
  61. Ramirez JM, Folkow LP, Blix AS (2007) Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Ann Rev Physiol 69:18.1–18.31Google Scholar
  62. Reed JZ, Butler PJ, Fedak MA (1994) The metabolic characteristics of the locomotory muscles of grey seals (Halichoerus grypus), harbour seals (Phoca vitulina), and Antarctic fur seals (Arctocephalus gazella). J Exp Biol 194:46Google Scholar
  63. Reynafarje B (1963) Simplified method for the determination of myoglobin. J Lab Clin Med 61:138–145Google Scholar
  64. Scholander PF (1940) Experimental investigations on the respiratory function in diving mammals and birds. Hval Skr 22:1–131Google Scholar
  65. Sivertsen E (1941) On the biology of the harp seal Phoca groenlandica Erx. Investigations carried out in the White Sea 1925–1937. Hval Skr 26:1–164Google Scholar
  66. Starck JM, Ricklefs RE (1998) Patterns of development: the altricial-precocoal spectrum. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial precocial spectrum. Oxford University Press, New York, pp 3–30Google Scholar
  67. Stewart REA, Lavigne DM (1980) Neonatal growth of northwest Atlantic Harp seals, Pagophilus groenlandicus. J Mammal 61(4):670–680CrossRefPubMedGoogle Scholar
  68. Suarez RK (1998) Oxygen and the upper limits to animal design and performance. J Exp Biol 201:1065–1072PubMedGoogle Scholar
  69. Terrados N, Jansson E, Sylven C, Kaijser L (1990) Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? J Appl Physiol 68:2369–2372PubMedGoogle Scholar
  70. Thorson PH, Le Boeuf BJ (1994) Developmental aspects of diving in Northern elephant seal pups. In: Le Boeuf BJ, Laws RM (eds) Elephant seals: population ecology, behavior, and physiology. University of California Press, Berkeley, pp 271–289Google Scholar
  71. Venters SJ, Thorsteinsdottir S, Duxson MJ (1999) Early development of the myotome in the mouse. Dev Dyn 216:219–232CrossRefPubMedGoogle Scholar
  72. Weise MJ, Costa DP (2007) Total body oxygen stores and physiological diving capacity of California sea lions as a function of sex and age. J Exp Biol 210:278–289CrossRefPubMedGoogle Scholar
  73. Williams TM, Davis RW, Fuiman LA, Francis J, Le Boeuf BJ, Horning M, Calambokidis J, Croll DA (2000) Sink or swim: strategies for cost-efficient diving by marine mammals. Science 288:133–136CrossRefPubMedGoogle Scholar
  74. Wittenberg JB, Wittenberg BA (2003) Myoglobin function reassessed. J Exp Biol 206:2011–2020CrossRefPubMedGoogle Scholar
  75. Worthy GAJ, Lavigne DM (1987) Mass loss, metabolic rate, and energy utilization by harp and gray seal pups during the postweaning fast. Physiol Zool 60:352–364Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Keri C. Lestyk
    • 1
    Email author
  • L. P. Folkow
    • 2
  • A. S. Blix
    • 2
  • M. O. Hammill
    • 3
  • J. M. Burns
    • 1
  1. 1.Department of Biological SciencesUniversity of Alaska AnchorageAnchorageUSA
  2. 2.Department of Arctic Biology, Institute of Medical BiologyUniversity of TromsøTromsøNorway
  3. 3.Maurice Lamontagne Institute, Fisheries and Oceans CanadaMont-JoliCanada

Personalised recommendations