Mammal-like muscles power swimming in a cold-water shark (original) (raw)

Nature volume 437, pages 1349–1352 (2005)Cite this article

Abstract

Effects of temperature on muscle contraction and powering movement are profound, outwardly obvious, and of great consequence to survival1,2. To cope with the effects of environmental temperature fluctuations, endothermic birds and mammals maintain a relatively warm and constant body temperature, whereas most fishes and other vertebrates are ectothermic and conform to their thermal niche, compromising performance at colder temperatures2,3. However, within the fishes the tunas and lamnid sharks deviate from the ectothermic strategy, maintaining elevated core body temperatures4,5 that presumably confer physiological advantages for their roles as fast and continuously swimming pelagic predators. Here we show that the salmon shark, a lamnid inhabiting cold, north Pacific waters, has become so specialized for endothermy that its red, aerobic, locomotor muscles, which power continuous swimming, seem mammal-like, functioning only within a markedly elevated temperature range (20–30 °C). These muscles are ineffectual if exposed to the cool water temperatures, and when warmed even 10 °C above ambient they still produce only 25–50% of the power produced at 26 °C. In contrast, the white muscles, powering burst swimming, do not show such a marked thermal dependence and work well across a wide range of temperatures.

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Acknowledgements

We thank the staff at the University of Alaska Seward Marine Center for the use of laboratory facilities, the captain and crew of the F/V Legend for their assistance in the fishing operations, and J. Valdez for logistical support. This work was supported by funding from the NSF and the University of California San Diego Academic Senate (R.E.S. and D.B.) and the NSERC (D.A.S.). Author Contributions All authors contributed equally to project planning, experimental work and writing of this Letter.

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Author notes

  1. Robert E. Shadwick
    Present address: Department of Zoology, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada

Authors and Affiliations

  1. Department of Biology, University of Massachusetts, Dartmouth, North Dartmouth, Massachusetts, 02747, USA
    Diego Bernal
  2. Marine Biology Research Division, Scripps Institution of Oceanography, California, 92093-0202, La Jolla, USA
    Diego Bernal & Robert E. Shadwick
  3. Department of Biological Sciences, Miracosta College, California, 92056, Oceanside, USA
    Jeanine M. Donley
  4. Department of Biological Sciences, University of Calgary, T2N 1N4, Alberta, Canada
    Douglas A. Syme

Authors

  1. Diego Bernal
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  2. Jeanine M. Donley
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  3. Robert E. Shadwick
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  4. Douglas A. Syme
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Corresponding authors

Correspondence toDiego Bernal or Robert E. Shadwick.

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Bernal, D., Donley, J., Shadwick, R. et al. Mammal-like muscles power swimming in a cold-water shark.Nature 437, 1349–1352 (2005). https://doi.org/10.1038/nature04007

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Editorial Summary

Sharks warm to the task

Whales are mammals and warm-blooded, sharks are fish and in the main cold-blooded. But in order to survive in the cold waters of the north Pacific Ocean, the salmon shark has become endothermic, maintaining a core body temperature that is higher than the surroundings, presumably a good move for animals that are continuously swimming. A study of salmon shark musculature shows that it is so specialized for endothermy that the red, aerobic muscles used for continuous swimming are remarkably mammal-like, functioning only within a narrow, elevated temperature range. These muscles are ineffectual if exposed to cool water, though the white muscles used for burst swimming work well in the cold. The red aerobic muscles in this shark mark it out from ‘ectothermic’ fish and are an evolutionary convergence with similarly endothermic tunas, and it seems that they have both edged towards mammals in the muscle stakes.