Changes in muscle composition during the development of diving ability in the Australian fur seal
Domenic A. LaRosa A , David J. Cannata A , John P. Y. Arnould A , Lynda A. O’Sullivan A , Rod J. Snow B and Jan M. West A C
+ Author Affiliations
- Author Affiliations
A School of Life and Environmental Sciences, Deakin University, Burwood, Vic. 3125, Australia.
B Centre for Physical Activity and Nutrition, Deakin University, Burwood, Vic. 3125, Australia.
C Corresponding author. Email: jan.west@deakin.edu.au
Submitted: 14 September 2011 Accepted: 23 July 2012 Published: 19 September 2012
Abstract
During development the Australian fur seal transitions from a terrestrial, maternally dependent pup to an adult marine predator. Adult seals have adaptations that allow them to voluntarily dive at depth for long periods, including increased bradycardic control, increased myoglobin levels and haematocrit. To establish whether the profile of skeletal muscle also changes in line with the development of diving ability, biopsy samples were collected from the trapezius muscle of pups, juveniles and adults. The proportions of different fibre types and their oxidative capacity were determined. Only oxidative fibre types (Type I and IIa) were identified, with a significant change in proportions from pup to adult. There was no change in oxidative capacity of Type I and IIa fibres between pups and juveniles but there was a two-fold increase between juveniles and adults. Myoglobin expression increased between pups and juveniles, suggesting improved oxygen delivery, but with no increase in oxidative capacity, oxygen utilisation within the muscle may still be limited. Adult muscle had the highest oxidative capacity, suggesting that fibres are able to effectively utilise available oxygen during prolonged dives. Elevated levels of total creatine in the muscles of juveniles may act as an energy buffer when fibres are transitioning from a fast to slow fibre type.
Additional keywords: creatine, skeletal muscle.
References
Andersen, H. T. (1966). Physiological adaptations in diving vertebrates. Physiological Reviews 46, 212–243.| 1:CAS:528:DyaF2sXmtlWgsw%3D%3D&md5=e7743759f695715caf52752df8f3aefeCAS |
Arnould, J. P. Y., and Hindell, M. A. (2001). Dive behaviour, foraging locations, and maternal-attendance patterns of Australian fur seals (Arctocephalus pusillus doriferus). Canadian Journal of Zoology 79, 35–48.
Billeter, R., Heizmann, C. W., Howald, H., and Jenny, E. (1981). Analysis of myosin light and heavy chain types in single human skeletal muscle fibers. European Journal of Biochemistry 116, 389–395.
| Analysis of myosin light and heavy chain types in single human skeletal muscle fibers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktVCjsbk%3D&md5=a7ed581e4afe1c72b28ce27243216578CAS |
Bonner, W. N. (1984). Lactation strategies in pinnipeds: problems for a marine mammal group. Symposium of the Zoological Society of London 51, 253–272.
Bredman, J. J., Weijs, W. A., Korfage, H. A. M., and Brugman Morrman, A. F. M. (1992). Myosin heavy chain expression in rabbit masseter muscle during postnatal development. Journal of Anatomy 180, 263–274.
| 1:CAS:528:DyaK38XlvVyrtbs%3D&md5=15e0eefdc350350a835f982a545b4c10CAS |
Brooke, M. H., and Kaiser, K. K. (1970). Three “myosin adenosine triphosphatase” systems: the nature of their pH liability and sulfhydryl dependence. The Journal of Histochemistry and Cytochemistry 18, 670–672.
| Three “myosin adenosine triphosphatase” systems: the nature of their pH liability and sulfhydryl dependence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXjvVCksQ%3D%3D&md5=4539aaa7daba5efddd801fdf790695d5CAS |
Burnette, W. N. (1981). “Western Blotting”: Electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Analytical Biochemistry 112, 195–203.
| “Western Blotting”: Electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXhvVOqtbs%3D&md5=e27da836a2172477a5caaceacb07fbdfCAS |
Burns, J. M. (1999). The development of diving behavior in juvenile Weddell seals: pushing physiological limits in order to survive. Canadian Journal of Zoology 77, 737–747.
| The development of diving behavior in juvenile Weddell seals: pushing physiological limits in order to survive.Crossref | GoogleScholarGoogle Scholar |
Burns, J., Lestyk, K., Folkow, L., Hammill, M., and Blix, A. (2007). Size and distribution of oxygen stores in harp and hooded seals from birth to maturity. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 177, 687–700.
| Size and distribution of oxygen stores in harp and hooded seals from birth to maturity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotVOitL0%3D&md5=d83169d4e7f4e71566cdd746a4238d0cCAS |
Burns, J. M., Skomp, N., Bishop, N., Lestyk, K., and Hammill, M. (2010). Development of aerobic and anaerobic metabolism in cardiac and skeletal muscles from harp and hooded seals. The Journal of Experimental Biology 213, 740–748.
| Development of aerobic and anaerobic metabolism in cardiac and skeletal muscles from harp and hooded seals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFSktrk%3D&md5=87a3fac8f6405cd2dca832d1770c34a0CAS |
Butler, P. J., and Jones, D. R. (1997). Physiology of diving birds and mammals. Physiological Reviews 77, 837–861.
| 1:STN:280:DyaK2sznvVartA%3D%3D&md5=143118109be928858af2a875b6f32eb9CAS |
Cannata, D. J., Ireland, Z., Dickinson, H., Snow, R. J., Russell, A. P., West, J. M., and Walker, D. W. (2010). Maternal creatine supplementation from mid-pregnancy protects the diaphragm of the newborn spiny mouse from intrapartum hypoxia-induced damage. Pediatric Research 68, 393–398.
| 1:CAS:528:DC%2BC3cXht1yqtrzK&md5=7a1b7db08a112bfdeca8444af7171bbdCAS |
Cannata, D. J., Crossley, K. J., Barclay, C. J., Walker, D. W., and West, J. M. (2011). Contribution of stretch to the change of activation properties of muscle fibers in the diaphragm at the transition from fetal to neonatal life. Frontiers of Physiology 2, 109.
| Contribution of stretch to the change of activation properties of muscle fibers in the diaphragm at the transition from fetal to neonatal life.Crossref | GoogleScholarGoogle Scholar |
Castellini, M. A., Somero, G. N., and Kooyman, G. L. (1981). Glycolytic enzyme activities in tissues of marine and terrestrial mammals. Physiological Zoology 54, 242–252.
| 1:CAS:528:DyaL3MXktVCjsb4%3D&md5=ccbf1169b809dcfeb6b50db1611576e7CAS |
Close, R. I. (1972). Dynamic properties of mammalian skeletal muscles. Physiological Reviews 52, 129–197.
| 1:STN:280:DyaE38%2FntVSntg%3D%3D&md5=19c6eb8ce0982a06c3f17e7261635d24CAS |
Costa, D., and Gales, N. (2000). Foraging energetics and diving behavior of lactating New Zealand sea lions, Phocarctos hookeri. The Journal of Experimental Biology 203, 3655–3665.
| 1:STN:280:DC%2BD3M%2FpvVarsg%3D%3D&md5=7bf1a23339f4e804975e2f6c1f56518eCAS |
Costa, D., Kuhn, C. E., Weise, M. J., Shaffer, S. A., and Arnould, J. P. Y. (2004). When does physiology limit foraging behaviour of freely diving mammals? International Congress Series 1275, 359–366.
| When does physiology limit foraging behaviour of freely diving mammals?Crossref | GoogleScholarGoogle Scholar |
Davis, R. W., and Kanatous, S. B. (1999). Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. The Journal of Experimental Biology 202, 1091–1113.
| 1:STN:280:DyaK1M3gtlGqug%3D%3D&md5=c745ec203bcc861b669d32de78010f26CAS |
Davis, R. W., Polasek, L., Watson, R., Fuson, A., Williams, T. M., and Kanatous, S. B. (2004). The diving paradox: new insights into the role of the dive response in air-breathing vertebrates. Comparative Biochemistry and Physiology. A. Comparative Physiology 138, 263–268.
Deacon, N., and Arnould, J. P. Y. (2009). Terrestrial apnoeas and the development of cardiac control in Australian fur seal (Arctocephalus pusillus doriferus) pups. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 179, 287–295.
| Terrestrial apnoeas and the development of cardiac control in Australian fur seal (Arctocephalus pusillus doriferus) pups.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3hs1ygtg%3D%3D&md5=06e73e2ee22c7d9c470761b4b13dbb27CAS |
Dolar, M. L. L., Suarez, P., Ponganis, P. J.,, and Kooyman, G. L. (1999). Myoglobin in pelagic small cetaceans. Journal of Experimental Biology 202, 227–236.
| 1:CAS:528:DyaK1MXhslOlsL0%3D&md5=eafc8592ffce0ce98fc625900372a5a9CAS |
dos Santos, R. A., Giannocco, G., and Nunes, M. T. (2001). Thyroid hormone stimulates myoglobin expression in soleus and extensorum digitalis longus muscles of rats: concomitant alterations in the activities of Krebs cycle oxidative enzymes. Thyroid 11, 545–550.
| Thyroid hormone stimulates myoglobin expression in soleus and extensorum digitalis longus muscles of rats: concomitant alterations in the activities of Krebs cycle oxidative enzymes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1egs7g%3D&md5=5974d4a4db228e075e31c83469a23d3dCAS |
Fowler, S. L., Costa, D. P., Arnould, J. P. Y., Gales, N. J., and Kuhn, C. E. (2006). Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer. Journal of Animal Ecology 75, 358–367.
| Ontogeny of diving behaviour in the Australian sea lion: trials of adolescence in a late bloomer.Crossref | GoogleScholarGoogle Scholar |
Fowler, S. L., Costa, D. P., Arnould, J. P. Y., Gales, N. J., and Burns, J. M. (2007). Ontogeny of oxygen stores and physiological diving capability in Australian sea lions. Functional Ecology 21, 922–935.
| Ontogeny of oxygen stores and physiological diving capability in Australian sea lions.Crossref | GoogleScholarGoogle Scholar |
Gros, G., Wittenberg, B. A., and Jue, T. (2010). Myoglobin’s old and new clothes: from molecular structure to function in living cells. The Journal of Experimental Biology 213, 2713–2725.
| Myoglobin’s old and new clothes: from molecular structure to function in living cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Olsr%2FN&md5=4f5415fa13bcd26269df6af598779b2fCAS |
Hämäläinen, N., and Pette, D. (1993). The histochemical profiles of fast fiber types IIB, IID and IIA in skeletal muscles of mouse, rat and rabbit. The Journal of Histochemistry and Cytochemistry 41, 733–743.
| The histochemical profiles of fast fiber types IIB, IID and IIA in skeletal muscles of mouse, rat and rabbit.Crossref | GoogleScholarGoogle Scholar |
Hoppeler, H., and Flück, M. (2002). Normal mammalian skeletal muscle and its phenotypic plasticity. The Journal of Experimental Biology 205, 2143–2152.
Hoppeler, H., and Vogt, M. (2001). Muscle adaptations to hypoxia. The Journal of Experimental Biology 204, 3133–3139.
| 1:STN:280:DC%2BD3MrjsVagtg%3D%3D&md5=e2d71bea6a554461b40a59f5cbd8cf16CAS |
in’t Zandt, H. J. A., de Groof, A. J. C., Renema, W. K. J., Oerlemans, F. T. J., Klomp, D. W. J., Wieringa, B., and Heerschap, A. (2003). Presence of (phospho)creatine in developing and adult skeletal muscle of mice without mitochondrial and cytosolic muscle creatine kinase isoforms. The Journal of Physiology 548, 847–858.
| Presence of (phospho)creatine in developing and adult skeletal muscle of mice without mitochondrial and cytosolic muscle creatine kinase isoforms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXls1KqsLg%3D&md5=19ea0b5908cf2deb83d4d92e197af8c0CAS |
Ipsiroglu, O. S., Stomberger, C., Ilas, J., HÃôger, H., MÃ1/4hl, A., and StÃôckler-Ipsiroglu, S. (2001). Changes in tissue creatine concentrations upon oral supplementation of creatine-monohydrate in various animal species. Life Sciences 69, 1805–1815.
| 1:CAS:528:DC%2BD3MXms12ktbY%3D&md5=dd1278b447708f1b0b8573774d4c3cf0CAS |
Ireland, Z., Russell, A. P., Walliman, T., Walker, D. W., and Snow, R. (2009). Developmental changes in the expression of creatine synthesizing enzymes and creatine transporter in a precocial rodent, the spiny mouse. BMC Developmental Biology 9, 39.
| Developmental changes in the expression of creatine synthesizing enzymes and creatine transporter in a precocial rodent, the spiny mouse.Crossref | GoogleScholarGoogle Scholar |
Jansson, E., and Sylvén, C. (1983). Myoglobin concentration in single type I and type II muscle fibres in man. Histochemistry 78, 121–124.
| Myoglobin concentration in single type I and type II muscle fibres in man.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXkt1Sjurk%3D&md5=998dc8af1e399c01c9cfd00e46e0cb6dCAS |
Kanatous, S. B., Davis, R. W., Watson, R., Polasek, L., Williams, T. M., and Mathieu-Costello, O. (2002). Aerobic capacities in the skeletal muscles of Weddell seals: key to longer dive durations? The Journal of Experimental Biology 205, 3601–3608.
| 1:CAS:528:DC%2BD3sXit1WhtQ%3D%3D&md5=e83f758e4a461ff89d7df1d0d7ee6f6dCAS |
Kanatous, S. B., Hawke, T. J., Trumble, S. J., Pearson, L. E., Watson, R. R., Garry, D. J., Williams, T. M., and Davis, R. W. (2008). The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals. The Journal of Experimental Biology 211, 2559–2565.
| The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1crgvVGksA%3D%3D&md5=7b7e0f12f1d54d64e0136867e5ea759aCAS |
Kanatous, S. B., Mammen, P. P. A., Rosenberg, P. B., Martin, C. M., White, M. D., DiMaio, J. M., Huang, G., Muallem, S., and Garry, D. J. (2009). Hypoxia reprograms calcium signaling and regulates myoglobin expression. American Journal of Physiology. Cell Physiology 296, C393–C402.
| Hypoxia reprograms calcium signaling and regulates myoglobin expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjtFGrs7Y%3D&md5=e6248d3eb8a372fbd2662c54ed9af388CAS |
Kooyman, G., Wahrenbrock, E., Castellini, M., Davis, R., and Sinnett, E. (1980). Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 138, 335–346.
| Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXmtVaju7o%3D&md5=f6d6acdb6e70b9e7111a53036954c6f9CAS |
Lefaucheur, L., Ecolan, P., Plantard, L., and Gueguen, N. (2002). New insights into muscle fiber types in the pig. The Journal of Histochemistry and Cytochemistry 50, 719–730.
| New insights into muscle fiber types in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1eks7Y%3D&md5=09be2824921fa24075b1b5482ecdc537CAS |
Lestyk, K., Folkow, L., Blix, A., Hammill, M., and Burns, J. (2009). Development of myoglobin concentration and acid buffering capacity in harp (Pagophilus groenlandicus) and hooded (Cystophora cristata) seals from birth to maturity. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 179, 985–996.
| Development of myoglobin concentration and acid buffering capacity in harp (Pagophilus groenlandicus) and hooded (Cystophora cristata) seals from birth to maturity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXht1OgtLrJ&md5=e8f6bd9207a99574b9ce8a3eab332b26CAS |
Littnan, C. L., and Arnould, J. P. Y. (2007). Effect of proximity to the shelf edge on the diet of female Australian fur seals. Marine Ecology Progress Series 338, 257–267.
| Effect of proximity to the shelf edge on the diet of female Australian fur seals.Crossref | GoogleScholarGoogle Scholar |
Liu, Y., Shen, T., Randall, W., and Schneider, M. (2005). Signaling pathways in activity-dependent fiber type plasticity in adult skeletal muscle. Journal of Muscle Research and Cell Motility 26, 13–21.
| Signaling pathways in activity-dependent fiber type plasticity in adult skeletal muscle.Crossref | GoogleScholarGoogle Scholar |
Lowry, O. H., and Passonneau, J. V. (1972). ‘A Flexible System of Enzymatic Analysis.’ (Academic Press: New York.)
Mänttäri, S., Anttila, K., and JÃÃrvilehto, M. (2008). Testosterone stimulates myoglobin expression in different muscles of the mouse. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 178, 899–907.
| Testosterone stimulates myoglobin expression in different muscles of the mouse.Crossref | GoogleScholarGoogle Scholar |
Noren, S. R., Iverson, S. J., and Boness, D. J. (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. Physiological and Biochemical Zoology 78, 482–490.
| 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.Crossref | GoogleScholarGoogle Scholar |
Peinado, B., Latorre, R., VáÂquez-Autón, J. M., Poto, A., Ramirez, G., López-Albors, O., Moreno, F., and Gil, F. (2004). Histochemical skeletal muscle fibre types in the sheep. Anatomia, Histologia, Embryologia 33, 236–243.
| Histochemical skeletal muscle fibre types in the sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czjslGksA%3D%3D&md5=56fbcceac06f224970175358f2040329CAS |
Perkoff, G. T., Hill, R. L., Brown, D. M., and Tyler, F. H. (1962). The characterization of adult human myoglobin. The Journal of Biological Chemistry 237, 2820–2827.
| 1:CAS:528:DyaF38Xks1Cgs7Y%3D&md5=e02f75f5a0dac345460b750970943586CAS |
Peter, J. B., Barnard, R. J., Edgerton, V. R., Gillespie, C. A., and Stempel, K. E. (1972). Metabolic profiles of three fibre types of skeletal muscle in guinea pigs and rabbits. Biochemistry 11, 2627–2633.
| Metabolic profiles of three fibre types of skeletal muscle in guinea pigs and rabbits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XksleisrY%3D&md5=e68ddc2480a598e283b99415cebb6bcbCAS |
Pette, D., and Staron, R. S. (1990). Cellular and molecular diversities of mammalian skeletal muscle fibres. Reviews of Physiology, Biochemistry and Pharmacology 116, 1–76.
| 1:STN:280:DyaK3M7ls12isA%3D%3D&md5=6b712f0756034005556b4d8a13669468CAS |
Pette, D., and Vrbová, G. (1985). Neural control of phenotypic expression in mammalian muscle fibers. Muscle & Nerve 8, 676–689.
| Neural control of phenotypic expression in mammalian muscle fibers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2FktVWktQ%3D%3D&md5=a80a7c68378bac9aba324a8654d2b7f3CAS |
Polasek, L., Dickson, K. A., and Davis, R. W. (2006). Metabolic indicators in the skeletal muscles of harbor seals (Phoca vitulina). American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 290, R1720–R1727.
| Metabolic indicators in the skeletal muscles of harbor seals (Phoca vitulina).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvVers74%3D&md5=83b690ea60cb34a804f82a5776f4f172CAS |
Ponganis, P. J., Welch, T. J., Welch, L. S., and Stockhard, T. H. (2010). Myoglobin production in emperor penguins. The Journal of Experimental Biology 213, 1901–1906.
| Myoglobin production in emperor penguins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlaltrc%3D&md5=cecbda9e84d4741f39b081ae1e03e9a4CAS |
Prewitt, J. S., Freistroffer, D. V., Schreer, J. F., Hammill, M. O., and Burns, J. M. (2010). Postnatal development of muscle biochemistry in nursing harbour seals (Phoca vitulina) pups: limitations to diving behaviour? Journal of Comparative Physiology 180, 757–766.
| 1:CAS:528:DC%2BC3cXmt1ems78%3D&md5=36102d9e75e171f1f7b2efe80e2bd96eCAS |
Reed, J. Z., Butler, P. J., and Fedak, M. A. (1994). The metabolic characteristics of the locomotory muscles of grey seals (Halichoerus grypus), harbour seals (Phoca vitulina) and Antarctic fur seals (Arctocephalus gazella). The Journal of Experimental Biology 194, 33–46.
| 1:STN:280:DyaK2M%2FltlKnug%3D%3D&md5=b5bfe38fcfaefa380bd57ad33cc6d6a8CAS |
Reynafarje, B. (1963). Simplified method for the determination of myoglobin. The Journal of Laboratory and Clinical Medicine 61, 138–145.
| 1:CAS:528:DyaF3sXktFSnu7Y%3D&md5=7463c3cd0a3a7172eed9fc52e2fd5bfbCAS |
Richmond, J., Burns, J., and Rea, L. (2006). Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus). Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 176, 535–545.
| Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus).Crossref | GoogleScholarGoogle Scholar |
Rico-Sanz, J., Thomas, E. L., Jenkinson, G., Mierisova, S., Iles, R., and Bell, J. D. (1999). Diversity in the levels of intracellular total creatine and triglycerides in human skeletal muscles observed by H-MRS. Journal of Applied Physiology 87, 2068–2072.
| 1:CAS:528:DC%2BD3cXlslemug%3D%3D&md5=be2ff3fef1cc5be906ce706204202755CAS |
Shero, M., Andrews, R., Lestyk, K., and Burns, J. (2012). Development of the aerobic dive limit and muscular efficiency in northern fur seals Callorhinus ursinus. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 182, 425–436.
| Development of the aerobic dive limit and muscular efficiency in northern fur seals Callorhinus ursinus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksVKnt7s%3D&md5=141390526da9ded129f28aa22dca6ae6CAS |
Spangenburg, E. E., and Booth, F. W. (2003). Molecular regulation of individual skeletal muscle fibre types. Acta Physiologica Scandinavica 178, 413–424.
| Molecular regulation of individual skeletal muscle fibre types.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1Crt7g%3D&md5=a2ae2d0f86afab3b22ad9c32223dcfefCAS |
Spence-Bailey, L. M., Verrier, D., and Arnould, J. P. Y. (2007). The physiological and behavioural development of diving in Australian fur seal (Arctocephalus pusillus doriferus) pups. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 177, 483–494.
| The physiological and behavioural development of diving in Australian fur seal (Arctocephalus pusillus doriferus) pups.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s3islWrtA%3D%3D&md5=b7f880212a4bc4cb5f4913b562132d44CAS |
Talmadge, R. J., and Roy, R. R. (1993). Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. Journal of Applied Physiology 75, 2337–2340.
| 1:CAS:528:DyaK2cXivFegtLo%3D&md5=1b5dbc6b6653887dbd42fb06ebed870fCAS |
Toniolo, L., Maccatrozzo, L., Patruno, M., Caliaro, F., Mascarello, F., and Reggiani, C. (2005). Expression of eight distinct MHC isoforms in bovine striated muscles: evidence for MHC-2B presence only in extraocular muscles. The Journal of Experimental Biology 208, 4243–4253.
| Expression of eight distinct MHC isoforms in bovine striated muscles: evidence for MHC-2B presence only in extraocular muscles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Ojug%3D%3D&md5=ba1e0ff4af1748c44c82f0112b3c3b2dCAS |
Trillmich, F. (1990). The behavioral ecology of maternal effort in fur seals and sea lions. Behaviour 114, 3–20.
| The behavioral ecology of maternal effort in fur seals and sea lions.Crossref | GoogleScholarGoogle Scholar |
Verrier, D., Guinet, C., Authier, M., Tremblay, Y., Shaffer, S., Costa, D. P., Groscolas, R., and Arnould, J. P. Y. (2011). Ontogeny of diving abilities in subantarctic fur seal pups: developmental trade-off in response to extreme fasting? Functional Ecology 25, 818–828.
| Ontogeny of diving abilities in subantarctic fur seal pups: developmental trade-off in response to extreme fasting?Crossref | GoogleScholarGoogle Scholar |
Walker, D. W., and Luff, A. R. (1995). Functional development of fetal limb muscles: a review of the roles of activity, nerves and hormones. Reproduction, Fertility and Development 7, 391–398.
| Functional development of fetal limb muscles: a review of the roles of activity, nerves and hormones.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK287oslCksA%3D%3D&md5=d5a5bf7a3ae926d16c00561a87b78f87CAS |
Wallimann, T., Wyss, M., Brdiczka, D., Nicolay, K., and Eppenberger, H. M. (1992). Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the ‘phosphocreatine circuit’ for cellular energy homeostasis. Biochemical Journal 281, 21–40.
| 1:CAS:528:DyaK38XjvVCjsA%3D%3D&md5=10d008599fcf80f7b6d75581a1221ca5CAS |
Watson, R. R., Miller, T. A., and Davis, R. W. (2003). Immunohistochemical fiber typing of harbor seal skeletal muscle. The Journal of Experimental Biology 206, 4105–4111.
| Immunohistochemical fiber typing of harbor seal skeletal muscle.Crossref | GoogleScholarGoogle Scholar |
Weise, M. J., and Costa, D. P. (2007). Total body oxygen stores and physiological diving capacity of California sea lions as a function of sex and age. The Journal of Experimental Biology 210, 278–289.
| Total body oxygen stores and physiological diving capacity of California sea lions as a function of sex and age.Crossref | GoogleScholarGoogle Scholar |
Wickham, L. L., Elsner, R., White, F. C., and Cornell, L. H. (1989). Blood viscosity in phocid seals: possible adaptations to diving. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 159, 153–158.
| Blood viscosity in phocid seals: possible adaptations to diving.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1MzktFSnsQ%3D%3D&md5=a918a85ee22fbacc8edf2c10b658e9e8CAS |
Wigston, D. J., and English, A. W. (1992). Fiber-type proportions in mammalian soleus muscle during postnatal developoment. Journal of Neurology 23, 61–70.
| 1:STN:280:DyaK383is1Ohug%3D%3D&md5=830df95b224fc7a98c82ac4e71e50101CAS |
Wittenberg, J. B. (1970). Myoglobin facilitated oxygen diffusion and the role of myoglobin in oxygen entry into muscle. Physiological Reviews 50, 559–636.
| 1:CAS:528:DyaE3MXhvFarsg%3D%3D&md5=24702499dbe0f1cc32720f2bdfa83722CAS |
Wu, J., Pieper, R., Wu, L., and Peters, J. (1989). Isolation and characterization of myoglobin and its two major isoforms from sheep heart. Clinical Chemistry 35, 778–782.
| 1:CAS:528:DyaL1MXktlKjtr0%3D&md5=3348c4614ebc32374e5d2472255fd7f8CAS |
Zar, J. H. (1984). ‘Biostatistical Analysis.’ (Prentice-Hall Inc.: Englewood Cliffs, NJ.)
