Skip to main content
SpringerLink
Log in

Postnatal development of muscle biochemistry in nursing harbor seal (Phoca vitulina) pups: limitations to diving behavior?

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Adult marine mammal muscles rely upon a suite of adaptations for sustained aerobic metabolism in the absence of freely available oxygen (O2). Although the importance of these adaptations for supporting aerobic diving patterns of adults is well understood, little is known about postnatal muscle development in young marine mammals. However, the typical pattern of vertebrate muscle development, and reduced tissue O2 stores and diving ability of young marine mammals suggest that the physiological properties of harbor seal (Phoca vitulina) pup muscle will differ from those of adults. We examined myoglobin (Mb) concentration, and the activities of citrate synthase (CS), β-hydroxyacyl coA dehydrogenase (HOAD), and lactate dehydrogenase (LDH) in muscle biopsies from harbor seal pups throughout the nursing period, and compared these biochemical parameters to those of adults. Pups had reduced O2 carrying capacity ([Mb] 28–41% lower than adults) and reduced metabolically scaled catabolic enzyme activities (LDH/RMR 20–58% and CS/RMR 29–89% lower than adults), indicating that harbor seal pup muscles are biochemically immature at birth and weaning. This suggests that pup muscles do not have the ability to support either the aerobic or anaerobic performance of adult seals. This immaturity may contribute to the lower diving capacity and behavior in younger pups. In addition, the trends in myoglobin concentration and enzyme activity seen in this study appear to be developmental and/or exercise-driven responses that together work to produce the hypoxic endurance phenotype seen in adults, rather than allometric effects due to body size.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agbulut O, Noirez P, Beaumont F, Butler-Browne G (2003) Myosin heavy chain isoforms in postnatal development of mice. Biol Cell 95:399–406

    Article  PubMed  CAS  Google Scholar 

  • Agüera E, Muñoz A, Castejón F, Essén-Gustavsson B (2001) Skeletal muscle fibre characteristics in young and old bulls and metabolic response after a bullfight. J Vet Med 48:313–319. doi:10.1046/j.1439-0442.2001.00362.x

    Google Scholar 

  • Baechler J, Beck CA, Bowen WD (2002) Dive shapes reveal temporal changes in the foraging behaviour of different age and sex classes of harbour seals (Phoca vitulina). Can J Zool 80:1569–1577. doi:10.1139/z02-150

    Article  Google Scholar 

  • Bangsbo J, Hellsten Y (1998) Muscle blood flow and oxygen uptake in recovery from exercise. Acta Physiol Scand 162:305–312. doi:10.1046/j.1365-201X.1998.0331e.x

    Article  PubMed  CAS  Google Scholar 

  • Bishop C, Butler P, Egginton S, El Haj A, Gabrielsen G (1995) Development of metabolic enzyme activity in locomotor and cardiac muscles of the migratory barnacle goose. Am J Physiol 269:R64–R72

    PubMed  CAS  Google Scholar 

  • Blaise Smith P (1980) Postnatal development of glycogen- and cyclic AMP-metabolizing enzymes in mammalian skeletal muscle. Biochim Biophys Acta 628:19–25

    Google Scholar 

  • Blix AS, Elsner RW, Kjekshus JK (1983) Cardiac output and its distribution through capillaries and A-V shunts in diving seals. Acta Physiol Scand 118:109–116. doi:10.1111/j.1748-1716.1983.tb07250.x

    Article  PubMed  CAS  Google Scholar 

  • Bowen WD, Harrison GD (1996) Offshore diet of grey seals Halichoerus grypus near Sable Island, Canada. Mar Ecol Prog Ser 112:1–11

    Article  Google Scholar 

  • Brooks GA, Fahey TD, Baldwin KM (2005) Exercise physiology. McGraw-Hill, New York

    Google Scholar 

  • Burns JM (1999) The development of diving behavior in juvenile Weddell seals: pushing physiological limits in order to survive. Can J Zool 77:737–747. doi:10.1139/cjz-77-5-737

    Article  Google Scholar 

  • Burns JM, Castellini MA (1996) Physiological and behavioral determinants of the aerobic dive limit in Weddell seal (Leptonychotes weddellii) pups. J Comp Phys B 166:473–483. doi:10.1007/BF02338290

    Article  Google Scholar 

  • Burns JM, Costa DP, Frost K, Harvey JT (2005) Development of body oxygen stores in harbor seals: effects of age, mass, and body composition. Physiol Biochem Zool 78:1057–1068. doi:10.1086/432922

    Article  PubMed  CAS  Google Scholar 

  • Burns JM, Lestyk KC, Folkow LP, Hammill MO, Blix AS (2007) Size and distribution of oxygen stores in harp and hooded seals from birth to maturity. J Comp Phys B 177:687–700. doi:10.1007/s00360-007-0167-2

    Article  CAS  Google Scholar 

  • Burns JM, Skomp N, Bishop N, Lestyk K, Hammill MO (2010) Development of aerobic and anaerobic metabolism in cardiac and skeletal muscles from harp and hooded seals. J Exp Biol (in press)

  • Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–899

    PubMed  CAS  Google Scholar 

  • Castellini MA (1991) The biology of diving mammals: behavioral, physiological and biochemical limits. In: Gilles R (ed) Advances in comparative and environmental physiology, 8th edn. Springer, Berlin, pp 105–134

    Google Scholar 

  • Castellini MA (1994) Apnea tolerance in the elephant seal during sleeping and diving: physiological mechanisms and correlations. In: LeBoeuf BJ, Laws RM (eds) Elephant seals: population ecology behavior and physiology. University of California Press, Berkeley, pp 343–353

    Google Scholar 

  • Castellini MA, Somero GN (1981) Buffering capacity of vertebrate muscle: correlations with potential for anaerobic function. J Comp Phys B 143:191–198

    Google Scholar 

  • Cherepanova V, Neshumova T, Elsner RW (1993) Muscle blood flow in diving mammals. Comp Biochem Physiol A 106:1–6

    Article  CAS  Google Scholar 

  • Choi IH, Ricklefs RE, Shea RE (1993) Skeletal muscle growth, enzyme activities, and the development of thermogenesis: a comparison between altricial and precocial birds. Physiol Zool 66:455–473

    CAS  Google Scholar 

  • 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 Phys B 177:217–227. doi:10.1007/s00360-006-0123-6

    Article  Google Scholar 

  • Condon K, Silberstein L, Blau HM, Thompson WJ (1990) Development of muscle fiber types in the prenatal rat hindlimb. Dev Biol 138:256–274

    Article  PubMed  CAS  Google Scholar 

  • Davis RW, Kanatous SB (1999) Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. J Exp Biol 202:1091–1113

    PubMed  CAS  Google Scholar 

  • Davis RW, Williams TM, Kooyman GL (1985) Swimming metabolism of yearling and adult harbor seals, Phoca vitulina. Physiol Zool 58:590–596

    Google Scholar 

  • Dearolf JL, McClelland BR, Dillaman RM, Frierson D, Pabst DA (2000) Precocial development of axial locomotor muscle in bottlenose dolphin (Tursiops truncatus). J Morphol 244:203–215. doi:10.1002/(SICI)1097-4687(200006)244:3<203:AID-JMOR5>3.0.CO;2-V

    Article  PubMed  CAS  Google Scholar 

  • Dietz MW, Ricklefs RE (1997) Growth rate and maturation of skeletal muscles over a size range of Galliform birds. Physiol Zool 70:502–510

    Article  PubMed  CAS  Google Scholar 

  • Dubé Y, Hammill MO, Barrette C (2003) Pup development and timing of pupping in harbour seals (Phoca vitulina) in the St Lawrence River Estuary, Canada. Can J Zool 81:188–194. doi:10.1139/z02-231

    Article  Google Scholar 

  • Elsner RW, Gooden B (1983) Diving and asphyxia: a comparative study of animals and man. Monogr Physiol Soc 40:1–168

    PubMed  CAS  Google Scholar 

  • Emmett B, Hochachka PW (1981) Scaling of oxidative and glycolytic enzymes in mammals. Respir Physiol 45:261–272

    Article  PubMed  CAS  Google Scholar 

  • Fluck M (2006) Functional, structural and molecular plasticity skeletal muscle in response to exercise stimuli. J Exp Biol 209:2239–2248. doi:10.1242/jeb.02149

    Article  PubMed  CAS  Google Scholar 

  • Frost KJ, Simpkins MA, Lowry LF (2001) Diving behavior of subadult and adult harbor seals in Prince William Sound, Alaska. Mar Mamm Sci 17:813–834. doi:10.1111/j.1748-7692.2001.tb01300.x

    Article  Google Scholar 

  • Frost KJ, Simpkins M, Small RJ, Lowry LF (2006) Development of diving by harbor seal pups in two regions of Alaska: use of the water column. Mar Mamm Sci 22:617–643. doi:10.1111/j.1748-7692.2006.00056.x

    Article  Google Scholar 

  • Garcia-Roves P, Huss JM, Han DH, Hancock CR, Iglesias-Gutierrez E, Chen M, Holloszy JO (2007) Raising plasma fatty acid concentration induces increased biogenesis of mitochondria in skeletal muscle. Proc Natl Acad Sci 104:10709–10713. doi:10.1073/pnas.0704024104

    Article  PubMed  CAS  Google Scholar 

  • Garry DJ, Bassel-Dubay R, Richarson JG, Neufer PD, Williams RS (1996) Postnatal development and plasticity of specialized fiber characteristics in the hindlimb. Dev Genet 19:146–156. doi:10.1002/(SICI)1520-6408(1996)19:2<146:AID-DVG6>3.0.CO;2-9

    Article  PubMed  CAS  Google Scholar 

  • Glatz J, Veerkamp J (1982) Postnatal development of palmitate oxidation and mitochondrial enzyme activities in rat cardiac and skeletal muscle. Biochim Biophys Acta 711:327–335

    PubMed  CAS  Google Scholar 

  • Goldspink G (1970) The proliferation of myofibrils during muscle fiber growth. J Cell Sci 6:593–603

    PubMed  CAS  Google Scholar 

  • Gondret F, Damon M, Jadhau S, Houdebine L, Herpin P, Hocquette J (2004) Age-related changes in glucose utilization and fatty acid oxidation in a muscle-specific manner during rabbit growth. J Muscle Res Cell Motil 25:405–410. doi:10.1007/s10974-004-2768-7

    Article  PubMed  CAS  Google Scholar 

  • Grand TI (1992) Altricial and precocial mammals: a model of neural and muscular development. Zoo Biol 11:3–15. doi:10.1002/zoo.1430110103

    Article  Google Scholar 

  • Greaves DK, Schreer JF, Hammill MO, Burns JM (2005) Diving heart rate development in postnatal harbour seals, Phoca vitulina. Physiol Biochem Zool 78:9–17. doi:10.1086/425201

    Article  PubMed  Google Scholar 

  • Griffiths RI, Baldwin J, Berger PJ (1994) Metabolic development of the sheep diaphragm during fetal and newborn life. Respir Phys 95:334–347

    Google Scholar 

  • Hochachka PW, Foreman RA (1993) Phocid and cetacean blueprints of muscle metabolism. Can J Zool 71:2089–2098. doi:10.1139/z93-294

    Article  CAS  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York

    Google Scholar 

  • Hochachka PW, Storey KB (1975) Metabolic consequences of diving in animals and man. Science 187:613–621. doi:10.1126/science.163485

    Article  PubMed  CAS  Google Scholar 

  • Hochachka P, Stanley C, Merkt J, Sumar-Kalinowski J (1983) Metabolic meaning of elevated levels of oxidative enzymes in high-altitude adapted animals: an interpretive hypothesis. Respir Physiol 52:303–313

    Article  PubMed  CAS  Google Scholar 

  • Hoppeler H, Fluck M (2002) Normal mammalian skeletal muscle and its phenotypic plasticity. J Exp Biol 205:2143–2152

    PubMed  Google Scholar 

  • Jorgensen C, Lydersen C, Kovacs KM (2001) Diving development in nursing harbour seal pups. J Exp Biol 204:3993–4004

    PubMed  CAS  Google Scholar 

  • Kanatous SB, DiMichele LV, Cowan DF, Davis RW (1999) High aerobic capacities in skeletal muscles of pinnipeds: adaptations to diving hypoxia. J Appl Physiol 86:1247–1256

    PubMed  CAS  Google Scholar 

  • 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 205:3601–3608

    PubMed  CAS  Google Scholar 

  • Kanatous SB, Hawke T, Trumble S, Pearson L, Watson R, Garry D, Williams T, Davis R (2008) The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals. J Exp Biol 211:2559–2565

    Article  PubMed  CAS  Google Scholar 

  • Kayar SR, Hoppeler H, Howald H, Claassen H, Oberholzer F (1986) Acute effects of endurance exercise on mitochondrial distribution and skeletal muscle morphology. Eur J Appl Physiol 54:578–584. doi:10.1007/BF00943344

    Article  CAS  Google Scholar 

  • Kelsen SG, Ference M, Kapoor S (1985) Effects of prolonged undernutrition on the structure and function of the diaphragm. J Appl Physiol 58:1354–1359

    Google Scholar 

  • Kooyman GL (1988) Diving physiology. Marine mammals. In: Wood SF (ed) Comparative pulmonary physiology: current concepts. Marcel-Dekker Inc, New York, pp 721–734

    Google Scholar 

  • Kooyman GL (1989) Diverse divers: physiology and behavior. Springer, Berlin

    Google Scholar 

  • Kooyman GL, Ponganis PJ (1998) The physiological basis of diving to depth: birds and mammals. Ann Rev Physiol 60:19–32. doi:10.1146/annurev.physiol.60.1.19

    Article  CAS  Google Scholar 

  • 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 Phys B 138:335–346. doi:10.1007/BF00691568

    Article  CAS  Google Scholar 

  • Kooyman GL, Castellini MA, Davis RW, Maue RA (1983) Aerobic diving limits of immature Weddell seals. J Comp Phys B 151:171–174. doi:10.1007/BF00689915

    Article  Google Scholar 

  • Krijgsveld K, Olson J, Ricklefs R (2001) Catabolic capacity of the muscles of shorebird chicks: maturation of function in relation to body size. Physiol Biochem Zool 74:250–260. doi:10.1086/319655

    Article  PubMed  CAS  Google Scholar 

  • Krustrup P, Söderlund K, Mohr M, Bangsbo J (2004) The slow component of oxygen uptake during intense, sub-maximal exercise in man is associated with additional fibre recruitment. Pflüg Arch Eur J Phys 447:855–866. doi:10.1007/s00424-003-1203-z

    Article  CAS  Google Scholar 

  • Lang SLC, Iverson SJ, Bowen WD (2005) Individual variation in milk composition over lactation in harbour seals (Phoca vitulina) and the potential consequences of intermittent attendance. Can J Zool 83:1525–1531. doi:10.1139/z05-149

    Article  CAS  Google Scholar 

  • Lapierre JL, Schreer JF, Burns JM, Hammill MO (2004) Developmental changes in cardiorespiratory patterns associated with terrestrial apnoeas in harbour seal pups. J Exp Biol 207:3891–3896. doi:10.1242/jeb.01222

    Article  PubMed  Google Scholar 

  • Lesage V, Hammill MO, Kovacs KM (1999) Functional classification of harbor seal (Phoca vitulina) dives using depth profiles, swim velocity, and an index of foraging success. Can J Zool 77:74–87. doi:10.1139/cjz-77-1-74

    Article  Google Scholar 

  • Longo LD, Koos BJ, Power GG (1973) Fetal myoglobin: quantitative determination and importance for oxygenation. Am J Physiol 224:1032–1036

    PubMed  CAS  Google Scholar 

  • Miller K, Irving L (1975) Metabolism and temperature regulation in young harbor seals, Phoca vitulina richardsi. Am J Physiol 229:506–511

    PubMed  CAS  Google Scholar 

  • Miller K, Rosenmann M, Morrison PR (1976) Oxygen uptake and temperature regulation of young harbor seals (Phoca vitulina richardsi) in water. Comp Biochem Physiol 54A:105–107

    Article  Google Scholar 

  • Miller WC, Bryce GR, Conlee RK (1984) Adaptations to a high fat diet that increase exercise endurance in male rats. J Appl Physiol 56:78–83

    PubMed  CAS  Google Scholar 

  • Muelbert MMC, Bowen WD (1993) Duration of lactation and postweaning changes in mass and body composition of harbour seal, Phoca vitulina, pups. Can J Zool 71:1405–1414. doi:10.1139/z93-194

    Article  Google Scholar 

  • Noren SR, Lacave G, Wells RS, Williams TM (2002) The development of blood oxygen stores in bottlenose dolphins (Tursiops truncatus): implications for diving capacity. J Zool 258:105–113. doi:10.1017/S0952836902001243

    Article  Google Scholar 

  • 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. Physiol Biochem Zool 78(4):482–490. doi:10.1086/430228

    Article  PubMed  Google Scholar 

  • Oftedal OT (2002) Use of maternal reserves as a lactation strategy in large mammals. Proc Nutr Soc 59:99–106. doi:10.1017/S0029665100000124

    Google Scholar 

  • Olson JM (2001) Ontogeny of catabolic and morphological properties of skeletal muscle of the red-winged blackbird (Agelaius phoeniceus). J Comp Phys B 171:527–542. doi:10.1007/s003600100202

    Article  CAS  Google Scholar 

  • Polasek LK, Davis RW (2001) Heterogeneity of myoglobin distribution in the locomotory muscles of five cetacean species. J Exp Biol 204:209–215

    PubMed  CAS  Google Scholar 

  • Polasek LK, Dickson KA, Davis RW (2006) Metabolic indicators in the skeletal muscles of harbor seals (Phoca vitulina). Am J Phys: Regul Int Comp Phys 290:R1720–R1727. doi:10.1152/ajpregu.00080.2005

    CAS  Google Scholar 

  • Ponganis PJ, Costello ML, Starke LN, Mathieu-Costello O, Kooyman GL (1997a) Structural and biochemical characteristics of locomotory muscles of emperor penguins, Aptenodytes forsteri. Respir Physiol 109:73–80. doi:10.1016/S0034-5687(97)84031-5

    Article  PubMed  CAS  Google Scholar 

  • Ponganis PJ, Kooyman GL, Winter LM, Starke LN (1997b) Heart rate and plasma lactate responses during submerged swimming and trained diving in California sea lions, Zalophus californianus. J Comp Phys B 167:9–16

    Article  CAS  Google Scholar 

  • Powers LV, Kandarian SC, Kunz TH (1991) Ontogeny of flight in the little brown bat, Myotis lucifugus: behavior, morphology, and muscle histochemistry. J Comp Physiol A 168:675–685. doi:10.1007/BF00224357

    Article  Google Scholar 

  • Rea LD, Costa DP (1992) Changes in standard metabolism during long-term fasting in northern elephant seal pups (Mirounga angustirostris). Physiol Zool 65:97–111

    Google Scholar 

  • 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 gazelle). J Exp Biol 194:33–46

    PubMed  CAS  Google Scholar 

  • Reynafarje B (1963) Simplified method for the determination of myoglobin. J Lab Clin Med 61:138–145

    CAS  Google Scholar 

  • Reynolds AJ, Taylor CR, Hoppeler H, Weibel ER, Weyand P, Roberts TJ, Reinhart G (2005) The effect of diet on sled dog performance, oxidative capacity, skeletal muscle microstructure, and muscle glycogen metabolism. In: Carey DP, Norton SA, Bolser SM (eds) Recent advances in canine and feline nutritional research. Orange Frazer Press, Wilmington, OH, pp 181–198

    Google Scholar 

  • Richmond JP, Burns JM, Rea LD (2006) Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus). J Comp Phys B 176:535–545

    Article  Google Scholar 

  • Saltin B, Gollnick P (1983) Skeletal muscle adaptability: significance for metabolism and performance. In: Peachey AR, Adrian RH (eds) Handbook of physiology, Section 10: skeletal muscle. American Physiological Society, Baltimore, pp 555–631

    Google Scholar 

  • Schiaffino S, Reggiani C (1994) Myosin isoforms in mammalian skeletal muscle. J Appl Physiol 77:493–501

    PubMed  CAS  Google Scholar 

  • Shea RE, Olson JM, Ricklefs RE (2007) Growth rate, protein accumulation, and catabolic enzyme activity of skeletal muscles of Galliform birds. Physiol Biochem Zool 80:306–316. doi:10.1086/512984

    Article  PubMed  CAS  Google Scholar 

  • Tipler TD, Edwards YH, Hopkinson DA (1978) Developmental changes in protein profiles of human cardiac and skeletal muscle. Ann Hum Genet 41:409–418. doi:10.1111/j.1469-1809.1978.tb00911.x

    Article  PubMed  CAS  Google Scholar 

  • Watson R, Miller TA, Davis RW (2003) Immunohistochemical fiber typing of harbor seal skeletal muscle. J Exp Biol 206:4105–4111

    Article  PubMed  Google Scholar 

  • Watson R, Kanatous SB, Cowan DF, Wen JW, Han VC, Davis RW (2007) Volume density and distribution of mitochondria in harbor seal (Phoca vitulina) skeletal muscle. J Comp Phys B 177:89–98. doi:10.1007/s00360-006-0111-x

    Article  Google Scholar 

  • Weller PA, Price M, Isenberg H, Edwards YH, Jeffreys AJ (1986) Myoglobin expression: early induction and subsequent modulation of myoglobin and myoglobin mRNA during myogenesis. Mol Cell Biochem 6:4539–4547

    CAS  Google Scholar 

  • Whipple GH (1926) The hemoglobin of striated muscle. Am J Physiol 76:693–707

    CAS  Google Scholar 

  • Williams TM, Dobson GP, Mathieu-Costello O, Morsbach D, Worley MB, Phillips JA (1997) Skeletal muscle histology and biochemistry of an elite sprinter, the African cheetah. J Comp Phys B 167:527–535. doi:10.1007/s003600050105

    Article  CAS  Google Scholar 

  • Winder W, Baldwin K, Holloszy J (1974) Enzymes involved in ketone utilization in different types of muscle: adaptation to exercise. Eur J Biochem 47:461–467. doi:10.1111/j.1432-1033.1974.tb03713.x

    Article  PubMed  CAS  Google Scholar 

  • Worthy GAJ, Lavigne DM (1987) Mass loss, metabolic rate, and energy utilization by harp and gray seal pups during the postweaning fast. Physiol Zool 60:352–364

    Google Scholar 

  • Zar JH (1984) Biostatistical analysis. Prentice-Hall, Englewood Cliffs, CA

    Google Scholar 

Download references

Acknowledgments

Many thanks to the 2000–2002 field crews for their hardwork and enthusiasm, most notably: P. Carter, D. Dion, Y. Dubé, J. Gosselin, D. Greaves, J. Greig, J. Lapierre, S. Turgeon, and G. Yunker. Thanks to L. Polasek for laboratory assistance. Funding for this work was provided by the Department of Fisheries and Oceans, Canada, the Natural Sciences and Engineering Research Council of Canada through an Operating Grant to JFS, and contributions from Alaska EPSCoR (NSF EPS-0346770) to JMB and JSP. Research protocols were approved by the Department of Fisheries and Oceans Canada, and the University of Alaska Anchorage Institutional Animal Care and Use Committee. Samples were imported under MMPA Permit # 1003-1646-00.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Alaska Anchorage, 3211 Providence Dr., Anchorage, AK, 99508, USA

    J. S. Prewitt & J. M. Burns

  2. Department of Life Sciences, Great Basin College, Elko, NV, 89801, USA

    D. V. Freistroffer

  3. Department of Biology, State University of New York Potsdam, Potsdam, NY, 13676, USA

    J. F. Schreer

  4. Maurice Lamontagne Institute, Fisheries and Oceans Canada, 850 route de la Mer, Mont-Joli, QC, G5H 3Z4, Canada

    M. O. Hammill

Authors
  1. J. S. Prewitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. V. Freistroffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. F. Schreer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. O. Hammill
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. M. Burns
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. S. Prewitt.

Additional information

Communicated by H. V. Carey.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Prewitt, J.S., Freistroffer, D.V., Schreer, J.F. et al. Postnatal development of muscle biochemistry in nursing harbor seal (Phoca vitulina) pups: limitations to diving behavior?. J Comp Physiol B 180, 757–766 (2010). https://doi.org/10.1007/s00360-010-0448-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-010-0448-z

Keywords

Search

Navigation