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First published online August 8, 2008
Journal of Experimental Biology 211, 2559-2565 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018119
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The ontogeny of aerobic and diving capacity in the skeletal muscles of Weddell seals

S. B. Kanatous1,*, T. J. Hawke2, S. J. Trumble3, L. E. Pearson1, R. R. Watson4, D. J. Garry5, T. M. Williams6 and R. W. Davis7

1 Department of Biology, Colorado State University, Fort Collins, CO 80523-1878, USA
2 School of Kinesiology and Health Science, York University, Toronto, ON, Canada M3J 1P3
3 Department of Biology, University of Michigan Flint, Flint, MI 48502, USA
4 Biological Sciences Department, California State Polytechnic University, Pomona, CA 91768, USA
5 Lillehei Heart Institute, University of Minnesota, Minneapolis, MN 55455, USA
6 Department of Ecology and Evolutionary Biology, University of California at Santa Cruz, Santa Cruz, CA 95060, USA
7 Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX 77551, USA


Figure 1
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Fig. 1. (A) The percentage of fast-oxidative fibers (Type IIA) increased significantly in the swimming muscle as seals matured and increased their dive durations. Histogram showing the change in fiber type composition (% of total fiber number), in the swimming (longissimus dorsi) muscles of Weddell seals as they mature. (B) The mitochondrial volume densities in the swimming muscles decreased as the seals matured. Histogram showing the decrease in the volume density of mitochondria in the swimming muscle of Weddell seals as they mature. Values are means ± s.e.m. (N=6). * denotes significantly different from the pups; {dagger} denotes significantly different from adults (P<0.05, ANOVA).

 

Figure 2
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Fig. 2. Plot of muscle mitochondrial volume density against body mass in athletic (filled circles) and sedentary terrestrial mammals (small dots) and pinnipeds (open circles). The linear relationship [y=6.75–1.34(log x), r2=0.70] was generated from the volume densities of the vastus medialis, a primary locomotory muscle, from various terrestrial mammals ranging in size from the dwarf mongoose to the steer (Kanatous et al., 1999Go) [terrestrial data from Hoppeler (Hoppeler et al., 1987)]. In contrast to the adult Weddell seals, whose mitochondrial volume densities are similar to that predicted for a sedentary terrestrial mammal of comparable size, juveniles and pups have mitochondrial volume densities similar to those of athletic terrestrial mammals and shorter-duration divers of similar size.

 

Figure 3
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Fig. 3. The concentration of myoglobin in the swimming muscles of different age classes of Weddell seals. The concentration of myoglobin was significantly higher in the swimming muscles of juveniles compared with either pups or adults. In addition, myoglobin concentration was also significantly higher in adults compared with pups. Values are means ± s.e.m. (N=6). * denotes significantly greater than pups; {dagger} denotes significantly greater than adults (P<0.05, ANOVA).

 

Figure 4
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Fig. 4. Histogram displaying the changes in the expression of calcium regulatory and responsive proteins that may influence the expression of myoglobin. Adult seals had the lowest relative protein expression and were significantly different from the juvenile in all but one (calsequestrin) of the proteins measured. Protein concentrations were similar in pups and juveniles in all proteins measured except myoglobin, which was significantly greater in the juvenile than either the pup or adult. Values are means ± s.e.m. (N=6). * denotes significantly different from pups; {dagger} denotes significantly greater than adults (P<0.05, ANOVA).

 

Figure 5
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Fig. 5. Summary reveals the ontogeny of skeletal muscle adaptations that enable long deep dives in Weddell seals. As newborn pups, Weddell seals have an extremely high aerobic capacity, similar to that found in terrestrial animal athletes and short-duration divers. However, this enhanced aerobic capacity is not an adaptation towards diving but is due to their high fat diet and the need to offset thermoregulatory costs associated with using their lanugo (natal fur) for insulation in the extremely harsh environment of Antarctica. As the pups begin to dive and mature into juveniles, their skeletal muscles begin to transform. As juveniles, they initiate the development of fast-oxidative fibers and significantly increase their intramuscular stores of oxygen in the form of oxymyoglobin. As they continue to mature and increase their diving capacity, Weddell seals increase their percentage of Type IIA fast-oxidative fibers in their skeletal muscles. In addition, their skeletal muscles transform to a more sedentary state in order to maintain low levels of aerobic metabolism under the hypoxic conditions associated with long-duration diving. Similar to what has been found in terrestrial mammals; the results of our subtractive hybridization analysis indicate that these changes in skeletal muscle metabolic potential are regulated by calcium signaling and its downstream mediator, calcineurin.

 

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© The Company of Biologists Ltd 2008