Skip to main content

Advertisement

Log in

Links between muscle phenotype and life history: differentiation of myosin heavy chain composition and muscle biochemistry in precocial and altricial pinniped pups

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

Abstract

In marine mammals, muscular development has been identified as a rate-limiting factor in achieving adult dive capacities. This study investigates the rate that myosin heavy chain (MHC) composition matures in a postural and locomotor skeletal muscle for four pinniped species with different lactation lengths: hooded seals, Cystophora cristata; harp seals, Pagophilus groenlandicus; northern fur seals, Callorhinus ursinus, and Steller sea lions, Eumetopias jubatus. The ontogeny of MHC isoform expression was compared with developmental rates of myoglobin concentrations, and aerobic (citrate synthase, β-hydroxyacyl-CoA dehydrogenase) and anaerobic (lactate dehydrogenase) enzyme activities. Within taxonomic families, species with shorter lactation periods had more mature muscles biochemically at birth, and fiber types differentiated earlier during ontogeny (Phocidae: hooded > harp seals, Otariidae: northern fur seals > Steller sea lions). Northern fur seal neonates had the most phenotypically-mature muscles in this study, with no immature MHC isoforms. The relationship between muscle biochemistry and MHC composition became more pronounced with age, and developed to reflect swimming mode and activity levels. In adults, phocids had more slow-twitch oxidative protein in their primary locomotor muscle, the Longissimus dorsi (LD), than otariids which likely reflects oxygen-sparing strategies for the phocids’ longer dives. Conversely, northern fur seal muscles had higher proportions of fast-twitch MHCs in the Pectoralis and LD, likely indicative of this species’ smaller size and higher mass-specific metabolic rates. Thus, muscle phenotype is linked with species life history, and a mismatch between muscle biochemistry and MHC composition at weaning has important implications for the first year of independent foraging in pinniped pups.

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

Access this article

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

CS:

Citrate synthase (IU g−1 wet tissue)

FOG:

Fast-twitch oxidative glycolytic

HOAD:

β-Hydroxyacyl-CoA dehydrogenase (IU g−1 wet tissue)

LD:

Longissimus dorsi

LDH:

Lactate dehydrogenase (IU g−1 wet tissue)

Mb:

Myoglobin (mg g−1 wet tissue)

MHC:

Myosin heavy chain

O2 :

Oxygen

Pec:

Pectoralis

PWF:

Post-weaning fast

SO:

Slow-twitch oxidative

References

  • Aarseth JJ, Nordoy ES, Blix AS (1999) The effect of body fat on basal metabolic rate in adult harp seals (Phoca groenlandicus). Comp Biochem Physiol 124:69–72

    CAS  Google Scholar 

  • Arnould JPY, Hindell MA (2001) Dive behaviour, foraging locations, and attendance patterns of Australian fur seals (Arctocphalus pusillus doriferus). Can J Zool 79:35–48

    Google Scholar 

  • Atkinson S, Arnould JPY, Mashburn KL (2011) Plasma cortisol and thyroid hormone concentrations in pre-weaning Australian fur seal pups. Gen Comp Endocrinol 172:277–281

    CAS  PubMed  Google Scholar 

  • Bajzak CE, Côté SD, Hammill MO, Stenson G (2009) Intersexual differences in the postbreeding foraging behaviour of the Northwest Atlantic hooded seal. Mar Ecol Prog Ser 385:285–294

    Google Scholar 

  • Baker JD, Donohue MJ (2000) Ontogeny of swimming and diving in northern fur seal (Callorhinus ursinus) pups. Can J Zool 78:100–109

    Google Scholar 

  • Baker JD, Thompson PM (2007) Temporal and spatial variation in age-specific survival rates of a long-lived mammal, the Hawaiian monk seal. Proc R Soc B Biol Sci 274(1608):407–415. https://doi.org/10.1098/rspb.2006.3737

    Article  Google Scholar 

  • Baldwin KM, Haddad F (2001) Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle. J Appl Physiol 90:345–357

    CAS  PubMed  Google Scholar 

  • Bass A, Brdiczka D, Eyer P, Hofer S, Pette D (1969) Metabolic differentiation of distinct muscle types at the level of enzymatic organization. Eur J Biochem 10(2):198–206

    CAS  PubMed  Google Scholar 

  • Beck CA, Bowen WD, Iverson SJ (2000) Seasonal changes in buoyancy and diving behaviour of adult grey seals. J Exp Biol 203:2323–2330

    CAS  PubMed  Google Scholar 

  • Blough ER, Rennie ER, Zhang F, Reiser PJ (1996) Enhanced electrophoretic separation and resolution of myosin heavy chains in mammalian and avian skeletal muscles. AnalBiochem 233:31–35

    CAS  Google Scholar 

  • Boily P (1996) Metabolic and hormonal changes during the molt of captive gray seals (Halichoerus grypus). Am J Physiol-Regul, Integr Comp Physiol 270(5):R1051–R1058. https://doi.org/10.1152/ajpregu.1996.270.5.R1051

    Article  CAS  Google Scholar 

  • Boily P, Lavigne DM (1997) Developmental and seasonal changes in resting metabolic rates of captive female grey seals. Can J Zool 75(11):1781–1789. https://doi.org/10.1139/z97-807

    Article  Google Scholar 

  • Bowen WD, Oftedal OT, Boness DJ (1985) Birth to weaning in four days: remarkable growth in the hooded seal, Cystophora cristata. Can J Zool 63:2841–2846

    Google Scholar 

  • Boyd IL (1998) Time and energy constraints in pinniped lactation. Am Nat 152(5):717–728

    CAS  PubMed  Google Scholar 

  • Boyd IL, Croxall JP (1992) Diving behaviour of lactating Antarctic fur seals. Can J Zool 70:919–928

    Google Scholar 

  • Burns JM, Castellini MA, Testa JW (1999) Movements and diving behavior of weaned Weddell seal (Leptonychotes weddellii) pups. Polar Biol 21:23–36

    Google Scholar 

  • Burns JM, Clark CA, Richmond JP (2004) The impact of lactation strategy on physiological development of juvenile marine mammals: implications for the transition to independent foraging. Int Congr Ser 1275:341–350. https://doi.org/10.1016/j.ics.2004.09.032

    Article  Google Scholar 

  • Burns JM, Costa DP, Frost KJ, Harvey JT (2005) Physiological development in juvenile harbor seals. Physiol Biochem Zool 78(6):1057–1068

    CAS  PubMed  Google Scholar 

  • 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 177:687–700

    CAS  PubMed  Google Scholar 

  • Burns JM, Lestyk K, Freistroffer D, Hammill MO (2015) Preparing muscles for diving: age-related changes in muscle metabolic profiles in Harp (Pagophilus groenlandicus) and Hooded (Cystophora cristata) seals. Physiol Biochem Zool 88(2):167–182

    CAS  PubMed  Google Scholar 

  • Butler PJ (2004) Metabolic regulation in diving birds and mammals. Respir Physiol Neurobiol 141(3):297–315. https://doi.org/10.1016/j.resp.2004.01.010

    Article  PubMed  Google Scholar 

  • Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77(3):837–899

    CAS  PubMed  Google Scholar 

  • Calkins DG, Pitcher KW (1982) Population assessment, ecology, and trophic relationships of Steller sea lions in the gulf of Alaska. Alaska Department of Fish and Game, Anchorage

    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(4):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 Physiol B 177(2):217–227. https://doi.org/10.1007/s00360-006-0123-6

    Article  PubMed  Google Scholar 

  • Close RI (1972) Dynamic properties of mammalian skeletal muscles. Physiol Rev 52(1):129–197

    CAS  PubMed  Google Scholar 

  • Condon K, Silberstein L, Blau HM, Thompson WJ (1990) Development of muscle fiber types in the prenatal rat hindlimb. DevBiol 138(2):256–274

    CAS  Google Scholar 

  • Costa DP, Shaffer SA (2012) Seabirds and marine mammals. In: Brown JH, Kodric-Brown A, Sibly RM (eds) Metabolic ecology: a scaling approach. John Wiley & Sons Ltd, Hoboken, pp 225–233

    Google Scholar 

  • Costa DP, Le Boeuf BJ, Ortiz CL, Huntley AC (1986) The energetics of lactation in the northern elephant seal, Mirounga angustirostris. J Zool Lond 209:21–33

    Google Scholar 

  • Cox V (2010) Thyroid hormone concentrations and their influence on thermoregulation in harp (Pagophilus groenlandicus) and hooded seals (Cystophora cristata). Thesis: Julius-Maximilians University Wurzburg, University of Alaska Anchorage

  • Crocker DE, Williams JD, Costa DP, Le Boeuf BJ (2001) Maternal traits and reproductive effort in northern elephant seals. Ecology 82:3541–3555

    Google Scholar 

  • d’Albis A, Janmot C, Couteaux R (1991) Species and muscle type dependence of perinatal isomyosin transitions. IntJDevBiol 35:53–56

    Google Scholar 

  • 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 Mol Integr Physiol 138(3):263–268. https://doi.org/10.1016/j.cbpb.2004.05.003

    Article  CAS  PubMed  Google Scholar 

  • De Miranda MA, Schlater AE, Green TL, Kanatous SB (2012) In the face of hypoxia: myoglobin increases in response to hypoxic conditions and lipid supplementation in cultured Weddell seal skeletal muscle cells. J Exp Biol 215(5):806–813. https://doi.org/10.1242/jeb.060681

    Article  CAS  PubMed  Google Scholar 

  • Derrickson EM (1992) Comparative reproductive strategies of altricial and precocial Eutherian mammals. Funct Ecol 6(1):57–65. https://doi.org/10.2307/2389771

    Article  Google Scholar 

  • Donohue MJ, Costa DP, Goebel ME, Baker JD (2000) The ontogeny of metabolic rate and thermoregulatory capabilities of Northern fur seal, Callorhinus ursinus, pups in air and water. J Exp Biol 203:1003–1016

    CAS  PubMed  Google Scholar 

  • dos Santos RA, Giannocco G, Nunes MT (2001) Thyroid hormone stimulations myoglobin expression in soleus and extensorum digitalis longus muscles of rats: concomitant alterations in the activities of krebs cycle oxidative enzymes. Thyroid 11(6):545–550

    PubMed  Google Scholar 

  • Elsner RW (1969) Cardiovascular adjustments to diving. In: Andersen HT (ed) The biology of marine mammals. Academic Press, New York, pp 117–146

    Google Scholar 

  • Flück M (2006) Functional, structural and molecular plasticity of mammalian skeletal muscle in response to exercise stimuli. J Exp Biol 209(Pt 12):2239–2248. https://doi.org/10.1242/jeb.02149

    Article  CAS  PubMed  Google Scholar 

  • Folkow LP, Blix AS (1999) Diving behaviour of hooded seals (Cystophora cristata) in the greenland and Norwegian Seas. Polar Biol 22(1):61–74. https://doi.org/10.1007/s003000050391

    Article  Google Scholar 

  • Folkow LP, Nordøy ES, Blix AS (2004) Distribution and diving behaviour of harp seals (Pagophilus groenlandicus) from the Greenland Sea stock. Polar Biol 27(5):281–298. https://doi.org/10.1007/s00300-004-0591-7

    Article  Google Scholar 

  • Folkow LP, Nordøy ES, Blix AS (2010) Remarkable development of diving performance and migrations of hooded seals (Cystophora cristata) during their first year of life. Polar Biol 33(4):433–441. https://doi.org/10.1007/s00300-009-0718-y

    Article  Google Scholar 

  • Fowler SL, Costa DP, Arnould JP, Gales NJ, Kuhn CE (2006) Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer. J Anim Ecol 75(2):358–367. https://doi.org/10.1111/j.1365-2656.2006.01055.x

    Article  PubMed  Google Scholar 

  • Geiseler SJ, Blix AS, Burns JM, Folkow LP (2013) Rapid postnatal development of myoglobin from large liver iron stores in hooded seals. J Exp Biol 216(10):1793–1798. https://doi.org/10.1242/jeb.082099

    Article  CAS  PubMed  Google Scholar 

  • Gentry RL, Kooyman GL, Goebel ME (1986) Feeding and diving behavior of northern fur seals. In: Gentry RL, Kooyman GL (eds) Fur seals: Maternal strategies on land and at sea. Princeton University Press, New Jersey, pp 61–78

    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

    PubMed  Google Scholar 

  • Haddad F, Roy RR, Edgerton VR, Baldwin KM (2003) Atrophy responses to muscle inactivity I: cellular markers of protein deficits. J Appl Physiol 95:781–790

    CAS  PubMed  Google Scholar 

  • Halvorsen S, Bechensteen AG (2002) Physiology of erythropoietin during mammalian development. Acta Paediatr Suppl 438:17–26

    Google Scholar 

  • Hastings KK (1996) Juvenile survival and maternal strategies of Weddell seals in McMurdo Sound, Antarctica. Thesis, University of Alaska, Fairbanks

  • Hastings KK, Frost KJ, Simpkins MA, Pendleton GW, Swain UG, Small RJ (2004) Regional differences in diving behavior of harbor seals in the Gulf of Alaska. Can J Zool 82:1755–1773

    Google Scholar 

  • Hastings KK, Jemison LA, Gelatt TS, Laake JL, Pendleton GW, King JC, Trites AW, Pitcher KW (2011) Cohort effects and spatial variation in age-specific survival of Steller sea lions from southeastern Alaska. Ecosphere 2(10):111. https://doi.org/10.1890/es11-00215.1

    Article  Google Scholar 

  • Hillier TA, Pedula KL, Schmidt MM, Mullen JA, Charles M-A, Pettitt DJ (2007) Childhood obesity and metabolic imprinting. Diabetes Care 30:2287–2292

    PubMed  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, New York

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hochachka PW, Gunga HC, Kirsch K (1998) Our ancestral physiological phenotype: an adaptation for hypoxia tolerance and for endurance performance? Proc Natl Acad Sci USA 95(4):1915–1920

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoopes LA, Rea LD, Rosen DA, Worthy GAJ (2004) Effects of body condition on resting metabolism in captive and free-ranging Steller sea lions (Eumetopias jubatus). Symp Comp Nutr Soc 5:79–82

    Google Scholar 

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

    PubMed  Google Scholar 

  • Hoppeler H, Vogt M (2001) Muscle tissue adaptations to hypoxia. J Exp Biol 204:3133–3139

    CAS  PubMed  Google Scholar 

  • Howell AB (1929) Anatomy of the eared and earless seals. Proc US Natl Mus 73:1–142

    Google Scholar 

  • Irving L, Scholander PF, Grinnell SW (1942) The regulation of arterial blood pressure in the seal during diving. Am J Physiol 135:557–566

    Google Scholar 

  • Kanatous SB (1997) High aerobic capacities in the skeletal muscles of seals, sea lions and fur seals: adaptations to diving hypoxia. Texas A&M University, Galveston

    Google Scholar 

  • Kanatous SB, Mammen PP (2010) Regulation of myoglobin expression. J Exp Biol 213(Pt 16):2741–2747. https://doi.org/10.1242/jeb.041442

    Article  CAS  PubMed  PubMed Central  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

    CAS  PubMed  Google Scholar 

  • Kanatous SB, Hawke TJ, Trumble SJ, Pearson LE, 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(Pt 16):2559–2565. https://doi.org/10.1242/jeb.018119

    Article  CAS  PubMed  Google Scholar 

  • Kooyman GL, Ponganis PJ (1998) The physiological basis of diving to depth: birds and mammals. Annu Rev Physiol 60:19–32

    CAS  PubMed  Google Scholar 

  • Kovacs KM, Lavigne DM (1992) Mass-transfer efficiency between hooded seal (Cystophora cristata) mothers and their pups in the Gulf of St. Lawrence. Can J Zool 70:1315–1320

    Google Scholar 

  • Kovacs KM, Lavigne DM, Innes S (1991) Mass transfer efficiency between harp seal (Phoca groenlandica) and their pups during lactation. J Zool Lond 223:213–221

    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(Pt 22):3891–3898. https://doi.org/10.1242/jeb.01222

    Article  PubMed  Google Scholar 

  • LaRosa DA, Cannata DJ, Arnould JPY, O’Sullivan LA, Snow RJ, West JM (2012) Changes in muscle composition during the development of diving ability in the Australian fur seal. J Aust J Zool 60(2):81–90. https://doi.org/10.1071/ZO11072

    Article  Google Scholar 

  • Lestyk KC, Folkow LP, Blix AS, Hammill MO, Burns JM (2009) Development of myoglobin concentration and acid buffering capacity in harp (Pagophilus groenlandicus) and hooded (Cystophora cristata) seals from birth to maturity. J Comp Physiol B 179(8):985–996. https://doi.org/10.1007/s00360-009-0378-9

    Article  CAS  PubMed  Google Scholar 

  • 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 49:424–430

    CAS  PubMed  Google Scholar 

  • Lydersen C, Kovacs KM (1996) Energetics of lactation in harp seals (Phoca groenlandica) from the Gulf of St. Lawrence, Canada. J Comp Physiol B 166:295–304

    CAS  PubMed  Google Scholar 

  • 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 167:81–88

    CAS  PubMed  Google Scholar 

  • Maltin C, Delday M, Sinclair K, Steven J, Sneddon A (2001) Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle. Reproduction 122(3):359–374. https://doi.org/10.1530/rep.0.1220359

    Article  CAS  PubMed  Google Scholar 

  • McLaren IA (1993) Growth in pinnipeds. BiolRev 68:1–79

    CAS  Google Scholar 

  • McPherron AC, Lee S-J (1997) Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci 94(23):12457–12461. https://doi.org/10.1073/pnas.94.23.12457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mellish JE, Iverson SJ, Bowen WD, Hammill MO (1999) Fat transfer and energetics during lactation in the hooded seal: the roles of tissue lipoprotein lipase in milk fat secretion and pup blubber deposition. J Comp Physiol B 169B:377–390

    Google Scholar 

  • Moore CD, Crocker DE, Fahlman A, Moore MJ, Willoughby DS, Robbins KA, Kanatous SB, Trumble SJ (2014) Ontogenetic changes in skeletal muscle fiber type, fiber diameter and myoglobin concentration in the Northern elephant seal (Mirounga angustirostris). Front Physiol. https://doi.org/10.3389/fphys.2014.00217

    Article  PubMed  PubMed Central  Google Scholar 

  • More O’Ferrall GJ, Cunningham EP (1974) Heritability of racing performance in thoroughbred horses. Livest Prod Sci 1(1):87–97. https://doi.org/10.1016/0301-6226(74)90092-X

    Article  Google Scholar 

  • Oftedal OT, Bowen WD, Widdowson EM, Boness DJ (1991) The prenatal molt and its ecological significance in hooded and harbor seals. Can J Zool 69:2489–2493

    Google Scholar 

  • Pettitt DJ, Knowler WC (1998) Long-term effects of the intrauterine environment, birth weight, and breast-feeding in Pima Indians. Diabetes Care 21(Suppl 2):B138–141

    PubMed  Google Scholar 

  • Ponganis PJ, Meir JU, Williams CL (2011) In pursuit of Irving and Scholander: a review of oxygen store management in seals and penguins. J Exp Biol 214(Pt 20):3325–3339. https://doi.org/10.1242/jeb.031252

    Article  CAS  PubMed  Google Scholar 

  • Prewitt JS, Freistroffer DV, Schreer JF, Hammill MO, Burns JM (2010) Postnatal development of muscle biochemistry in nursing harbor seal (Phoca vitulina) pups: limitations to diving behavior? J Comp Physiol B 180(5):757–766

    CAS  PubMed  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 gazella). J Exp Biol 194:33–46

    CAS  PubMed  Google Scholar 

  • Rehberg MJ, Burns JM (2008) Differences in diving and swimming behavior of pup and juvenile Steller sea lions (Eumetopias jubatus) in Alaska. Can J Zool 86:539–553

    Google Scholar 

  • Rehberg MJ, Andrews RD, Swain UG, Calkins DG (2009) Foraging behavior of adult female Steller sea lions during the breeding season in Southeast Alaska. Mar Mamm Sci 25:588–604

    Google Scholar 

  • Reiser PJ, Kline WO (1998) Electrophoretic separation and quantitation of cardiac myosin heavy chain isoforms in eight mammalian species. Am J Physiol 274:H1048–H1053

    CAS  PubMed  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 Physiol B 176(6):535–545. https://doi.org/10.1007/s00360-006-0076-9

    Article  PubMed  Google Scholar 

  • Ricklefs RE, Shea RE, Choi IH (1994) Inverse relationship between functional maturity and exponential growth rate of avian skeletal muscle: a constraint on evolutionary response. Evolution 48(4):1080–1088

    PubMed  Google Scholar 

  • Robinson PW, Costa DP, Crocker DE, Gallo-Reynoso JP, Champagne CD, Fowler MA, Goetsch C, Goetz KT, Hassrick JL, Huckstadt LA, Kuhn CE, Maresh JL, Maxwell SM, McDonald BI, Peterson SH, Simmons SE, Teutschel NM, Villegas-Amtmann S, Yoda K (2012) Foraging behavior and success of a mesopelagic predator in the northeast Pacific Ocean: insights from a data-rich species, the northern elephant seal. PLoS One 7(5):e36728

    CAS  PubMed  PubMed Central  Google Scholar 

  • Scholander PF (1963) The master switch of life. Sci Am 209:92–106

    CAS  PubMed  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(3):306–316

    CAS  PubMed  Google Scholar 

  • Shero MR, Andrews RD, Lestyk KC, Burns JM (2012) Development of the aerobic dive limit and muscular efficiency in northern fur seals (Callorhinus ursinus). J Comp Physiol B 182:425–436

    CAS  PubMed  Google Scholar 

  • Shero MR, Costa DP, Burns JM (2015) Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities. J Comp Physiol B 185(7):811–824

    CAS  PubMed  Google Scholar 

  • Shero MR, Goetz KT, Costa DP, Burns JM (2018) Temporal changes in Weddell seal dive behavior over winter: Are females increasing foraging effort to support gestation? Ecol Evol 8(23):11857–11874. https://doi.org/10.1002/ece3.4643

    Article  PubMed  PubMed Central  Google Scholar 

  • Singer D, Mühlfeld C (2007) Perinatal adaptation in mammals: the impact of metabolic rate. Comp Biochem Physiol A Mol Integr Physiol 148(4):780–784. https://doi.org/10.1016/j.cbpa.2007.05.004

    Article  CAS  PubMed  Google Scholar 

  • Sivertsen E (1941) On the biology of the harp seal Phoca groenlandica Erx. Investigations carried out in the White Sea 1925–1937. Hvalradets Skrifter, Norske Videnskamp-Akad, Oslo 26:1–164

    Google Scholar 

  • Somo DA, Ensminger DC, Sharick JT, Kanatous SB, Crocker DE (2015) Development of dive capacity in northern elephant seals (Mirounga angustirostris): reduced body reserves at weaning are associated with elevated body oxygen stores during the postweaning fast. Physiol Biochem Zool 88(5):471–482

    PubMed  Google Scholar 

  • Spence-Bailey LM, Verrier D, Arnould JP (2007) The physiological and behavioural development of diving in Australian fur seal (Arctocephalus pusillus doriferus) pups. J Comp Physiol B 177(4):483–494. https://doi.org/10.1007/s00360-007-0146-7

    Article  CAS  PubMed  Google Scholar 

  • Stirling I (1977) Adaptations of Weddell and ringed seals to exploit the polar fast ice habitat in the absence or presence of surface predators. In: Llano GA (ed) Adaptations within Antarctic ecosystems. Proceedings of the 3rd SCAR Symposium on Antarctic Biology. Smithsonian Institute, Washington DC, pp 741–748

  • Walker DW, Luff AR (1995) Functional development of fetal limb muscles: a review of the roles of activity, nerves and hormones. Reprod Fertil Dev 7(3):391–398

    CAS  PubMed  Google Scholar 

  • Wegner J, Albrecht E, Fiedler I, Teuscher F, Papstein HJ, Ender K (2000) Growth- and breed-related changes of muscle fiber characteristics in cattle. J Anim Sci 78(6):1485–1496. https://doi.org/10.2527/2000.7861485x

    Article  CAS  PubMed  Google Scholar 

  • Wheatley KE, Bradshaw CJ, Davis LS, Harcourt RG, Hindell MA (2006) Influence of maternal mass and condition on energy transfer in Weddell seals. J Anim Ecol 75(3):724–733. https://doi.org/10.1111/j.1365-2656.2006.01093.x

    Article  PubMed  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(3):352–364

    Google Scholar 

Download references

Acknowledgements

Samples were collected with the Canadian Department of Fisheries and Oceans (harp and hooded seals; sampling conducted under IML-2007-004 to Canadian DFO, import under NMFS MMPA No. 782-1694-02), the Alaska SeaLife Center and North Pacific Wildlife Consulting LLC (northern fur seal samples; research authorized by permit No. 04-1370 from the Sakhalin-Kuril Territorial Department of the Federal Committee of Fisheries of Russia, import under NMFS MMPA No. 881-1724), and the Alaska Department of Fish and Game and National Marine Mammal Laboratory (Steller sea lions; sample collection under NMFS MMPA No. 358-1564 (ADF&G) and 782-1532 (NMML)), and respective Institutional Animal Care and Use Committees. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE-1242789 to M.R.S., the Research Experience for Undergraduates program to L.S. under DBI-1263415, and material is based upon work, while J.M.B. was serving at the National Science Foundation. Any opinion, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michelle R. Shero.

Additional information

Communicated by G. Heldmaier.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shero, M.R., Reiser, P.J., Simonitis, L. et al. Links between muscle phenotype and life history: differentiation of myosin heavy chain composition and muscle biochemistry in precocial and altricial pinniped pups. J Comp Physiol B 189, 717–734 (2019). https://doi.org/10.1007/s00360-019-01240-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-019-01240-w

Keywords

Navigation