Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

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

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

Australian Journal of Zoology 60(2) 81-90 https://doi.org/10.1071/ZO11072
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 | open url image1

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. open url image1

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 | 1:CAS:528:DyaL3MXktVCjsbk%3D&md5=a7ed581e4afe1c72b28ce27243216578CAS | open url image1

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 | open url image1

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 | 1:CAS:528:DyaE3MXjvVCksQ%3D%3D&md5=4539aaa7daba5efddd801fdf790695d5CAS | open url image1

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 | 1:CAS:528:DyaL3MXhvVOqtbs%3D&md5=e27da836a2172477a5caaceacb07fbdfCAS | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD2sXotVOitL0%3D&md5=d83169d4e7f4e71566cdd746a4238d0cCAS | open url image1

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 | 1:CAS:528:DC%2BC3cXlsFSktrk%3D&md5=87a3fac8f6405cd2dca832d1770c34a0CAS | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

Close, R. I. (1972). Dynamic properties of mammalian skeletal muscles. Physiological Reviews 52, 129–197.
| 1:STN:280:DyaE38%2FntVSntg%3D%3D&md5=19c6eb8ce0982a06c3f17e7261635d24CAS | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

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. open url image1

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 | 1:STN:280:DC%2BD1M3hs1ygtg%3D%3D&md5=06e73e2ee22c7d9c470761b4b13dbb27CAS | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD3MXlt1egs7g%3D&md5=5974d4a4db228e075e31c83469a23d3dCAS | open url image1

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 | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BC3cXht1Olsr%2FN&md5=4f5415fa13bcd26269df6af598779b2fCAS | open url image1

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 | open url image1

Hoppeler, H., and Flück, M. (2002). Normal mammalian skeletal muscle and its phenotypic plasticity. The Journal of Experimental Biology 205, 2143–2152. open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD3sXls1KqsLg%3D&md5=19ea0b5908cf2deb83d4d92e197af8c0CAS | open url image1

Ipsiroglu, O. S., Stomberger, C., Ilas, J., HÇôger, H., MÇ1/4hl, A., and StÇôckler-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 | open url image1

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 | open url image1

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 | 1:CAS:528:DyaL3sXkt1Sjurk%3D&md5=998dc8af1e399c01c9cfd00e46e0cb6dCAS | open url image1

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 | open url image1

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 | 1:STN:280:DC%2BD1crgvVGksA%3D%3D&md5=7b7e0f12f1d54d64e0136867e5ea759aCAS | open url image1

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 | 1:CAS:528:DC%2BD1MXjtFGrs7Y%3D&md5=e6248d3eb8a372fbd2662c54ed9af388CAS | open url image1

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 | 1:CAS:528:DyaL3cXmtVaju7o%3D&md5=f6d6acdb6e70b9e7111a53036954c6f9CAS | open url image1

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 | 1:CAS:528:DC%2BD38Xjt1eks7Y%3D&md5=09be2824921fa24075b1b5482ecdc537CAS | open url image1

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 | 1:CAS:528:DC%2BD1MXht1OgtLrJ&md5=e8f6bd9207a99574b9ce8a3eab332b26CAS | open url image1

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 | open url image1

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 | open url image1

Lowry, O. H., and Passonneau, J. V. (1972). ‘A Flexible System of Enzymatic Analysis.’ (Academic Press: New York.)

Mänttäri, S., Anttila, K., and JÇÏrvilehto, 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 | open url image1

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 | open url image1

Peinado, B., Latorre, R., Vá­quez-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 | 1:STN:280:DC%2BD2czjslGksA%3D%3D&md5=56fbcceac06f224970175358f2040329CAS | open url image1

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 | open url image1

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 | 1:CAS:528:DyaE38XksleisrY%3D&md5=e68ddc2480a598e283b99415cebb6bcbCAS | open url image1

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 | open url image1

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 | 1:STN:280:DyaL28%2FktVWktQ%3D%3D&md5=a80a7c68378bac9aba324a8654d2b7f3CAS | open url image1

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 | 1:CAS:528:DC%2BD28XlvVers74%3D&md5=83b690ea60cb34a804f82a5776f4f172CAS | open url image1

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 | 1:CAS:528:DC%2BC3cXptlaltrc%3D&md5=cecbda9e84d4741f39b081ae1e03e9a4CAS | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BC38XksVKnt7s%3D&md5=141390526da9ded129f28aa22dca6ae6CAS | open url image1

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 | 1:CAS:528:DC%2BD3sXmt1Crt7g%3D&md5=a2ae2d0f86afab3b22ad9c32223dcfefCAS | open url image1

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 | 1:STN:280:DC%2BD2s3islWrtA%3D%3D&md5=b7f880212a4bc4cb5f4913b562132d44CAS | open url image1

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 | open url image1

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 | 1:CAS:528:DC%2BD28Xjs1Ojug%3D%3D&md5=ba1e0ff4af1748c44c82f0112b3c3b2dCAS | open url image1

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 | open url image1

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 | open url image1

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 | 1:STN:280:DyaK287oslCksA%3D%3D&md5=d5a5bf7a3ae926d16c00561a87b78f87CAS | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

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 | 1:STN:280:DyaL1MzktFSnsQ%3D%3D&md5=a918a85ee22fbacc8edf2c10b658e9e8CAS | open url image1

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 | open url image1

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 | open url image1

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 | open url image1

Zar, J. H. (1984). ‘Biostatistical Analysis.’ (Prentice-Hall Inc.: Englewood Cliffs, NJ.)



Rent Article (via Deepdyve) Export Citation Cited By (3)