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.
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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
References
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)
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
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 495:587–596
Bate Smith EC (1938) The buffering of muscle in rigor: protein, phosphate and carnosine. J Physiol 92:336–343
Blix AS, Steen JB (1979) Temperature regulation in newborn polar homeotherms. Physiol Rev 59:285–304
Bodkin JL, Esslinger GJ, Monson DH (2004) Foraging depths of sea otters and implications to costal marine communities. Mar Mamm Sci 20:305–321
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 65:1–8
Bowen WD, Boness DJ, Iverson SJ (1999) Diving behaviour of lactating harbour seals and their pups during maternal foraging trips. Can J Zool 77:978–988
Brooks GA, Fahey TD, Baldwin KM (2005) Exercise physiology, 4th edn. McGraw-Hill, New York
Bryden MM (1972) Body size and composition of elephant seals Mirounga leonina: absolute measurements and estimates from bone dimensions. J Zool Lond 167:265–276
Burns JM, Costa DP, Frost KJ, Harvey JT (2005) Physiological development in juvenile harbor seals. Phys Bioch Zool 78:1057–1068
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
Burton RF (1978) Intracellular buffering. Respir Physiol 33:51–58
Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–899
Carrier DR (1983) Postnatal ontogeny of the musculo-skeletal system in the black-tailed jack rabbit (Lepus californicus). J Zool 201:27–55
Castellini MA, Somero GN (1981) Buffering capacity of vertebrate muscle: correlations with potential for anaerobic function. J Comp Physiol 143:191–198
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 177:217–227
Close RI (1972) Dynamic properties of mammalian skeletal muscles. Physiol Rev 52:129–197
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 138:263–268
Evans BK, Jones DR, Baldwin J, Gabbott GRJ (1994) Diving ability of the platypus. Aust J Zool 42:17–27
Fish FE, Ronald SI (1988) Kinematics and estimated thrust production of swimming harp and ringed seals. J Exp Biol 137:157–173
Folkow LP, Blix AS (1999) Diving behaviour of hooded seals (Cystophora cristata) in the Greenland and Norwegian Seas. Polar Biol 22:61–74
Folkow LP, Nordoy ES, Blix AS (2004) Distribution and diving behavior of harp seals (Pagophilus groenlandica) from the Greenland Sea stock. Polar Biol 27:281–298
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 19:146–156
George JC, Ronald K (1975) Metabolic adaptation in pinniped skeletal muscle. Rapp P -v Reun Cons int Explor Mer 169:432–436
Grand TI (1977) Body weight: its relation to tissue composition, segment distribution, and motor function. Am J Phys Anthrop 47:211–240
Grand TI, Barboza PS (2001) Anatomy and development of the koala, Phascolarctos cinereus: an evolutionary perspective on the superfamily Vombatoidea. Anat Embryol 203:211–223
Greaves DK, Schreer JF, Hammill MO, Burns JM (2005) Diving heart rate development in postnatal harbour seals, Phoca vitulina. Phys Bioch Zool 78:9–17
Hochachka PW, Foreman RA (1993) Phocid and cetacean blueprints of muscle metabolism. Can J Zool 71:2089–2098
Holloszy JO, Booth FW (1976) Biochemical adaptations to endurance exercise in muscle. Ann Rev Physiol 38:273–291
Howell AB (1929) Anatomy of the eared and earless seals. Proc U S Natl Mus 73:1–142
Jamon M (2006) The early development of motor control in neonate rat. Evol 5:657–666
Jorgensen C, Lydersen C, Kovacs KM (2001) Diving development in nursing harbour seal pups. J Exp Biol 204:3993–4004
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
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
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 211:2559–2565
Kooyman GL (1989) Diverse divers: physiology and behavior. Springer, Berlin
Kooyman GL, Castellini MA, Davis RW (1981) Physiology of diving in marine mammals. Ann Rev Physiol 43:343–356
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 62:143–163
Kovacs KM, Lavigne DM (1986) Maternal investment and neonatal growth in phocid seals. J Anim Ecol 55:1035–1051
Kristensen M, Albertsen J, Rentsch M, Juel C (2005) Lactate and force production in skeletal muscle. J Physiol 562:521–526
Lenfant C, Johansen K, Torrance JD (1970) Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir Physiol 9:277–286
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
Lydersen C, Ryg MS, Hammill MO, O’Brien J (1992) Oxygen stores and aerobic dive limit of ringed seals (Phoca hispida). Can J Zool 70:458–461
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
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 74:178–190
Merrick RL, Loughlin TR (1997) Foraging behavior of adult female and young-of-the-year Steller sea lions in Alaskan waters. Can J Zool 75:776–786
Muir GD (2000) Early ontogeny of locomotor behavior: a comparison between altricial and precocial animals. Brain Res Bull 53:719–726
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 31:1119–1135
Noren SR (2004) Buffering capacity of the locomotor muscle in cetaceans: correlates with postpartum development, dive duration, and swim performance. Mar Mamm Sci 20:808–822
Noren SR, Williams TM (2000) Body size and skeletal muscle myoglobin of cetaceans: adaptations for maximizing dive duration. Comp Biochem Physiol A 126:181–191
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 171:127–134
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 78:482–490
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 69:635–657
Ontell M, Dunn RF (1978) Neonatal muscle growth: a quantitative study. Am J Anat 152:539–555
Peronnet F, Aguilaniu B (2006) Lactic acid buffering, nonmetabolic CO2 and exercise hyperventilation: A critical reappraisal. Respir Physiol Neurobiol 150:4–18
Pette D, Staron RS (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 116:1–76
Picard B, Lefaucheur L, Berri C, Duclos MJ (2002) Muscle fibre ontogenesis in farm animal species. Reprod Nutr Dev 42:415–431
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 109:73–80
Ponganis PJ, Starke LN, Horning M, Kooyman GL (1999) Development of diving capacity in emperor penguins. J Exp Biol 202:781–786
Ramirez JM, Folkow LP, Blix AS (2007) Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Ann Rev Physiol 69:18.1–18.31
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 194:46
Reynafarje B (1963) Simplified method for the determination of myoglobin. J Lab Clin Med 61:138–145
Scholander PF (1940) Experimental investigations on the respiratory function in diving mammals and birds. Hval Skr 22:1–131
Sivertsen E (1941) On the biology of the harp seal Phoca groenlandica Erx. Investigations carried out in the White Sea 1925–1937. Hval Skr 26:1–164
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 3–30
Stewart REA, Lavigne DM (1980) Neonatal growth of northwest Atlantic Harp seals, Pagophilus groenlandicus. J Mammal 61(4):670–680
Suarez RK (1998) Oxygen and the upper limits to animal design and performance. J Exp Biol 201:1065–1072
Terrados N, Jansson E, Sylven C, Kaijser L (1990) Is hypoxia a stimulus for synthesis of oxidative enzymes and myoglobin? J Appl Physiol 68:2369–2372
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 271–289
Venters SJ, Thorsteinsdottir S, Duxson MJ (1999) Early development of the myotome in the mouse. Dev Dyn 216:219–232
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 210:278–289
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 288:133–136
Wittenberg JB, Wittenberg BA (2003) Myoglobin function reassessed. J Exp Biol 206:2011–2020
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
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.
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Communicated by H. V. Carey.
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Lestyk, K.C., Folkow, L.P., Blix, A.S. et al. 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, 985–996 (2009). https://doi.org/10.1007/s00360-009-0378-9
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DOI: https://doi.org/10.1007/s00360-009-0378-9