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Mammal-like muscles power swimming in a cold-water shark

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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Figure 1: Thermal gradients superimposed on a three-dimensional map of RM and WM distribution in salmon sharks ( Lamna ditropis).
Figure 2: Muscle twitch duration at different temperatures.
Figure 3: Relative power output in myotomal muscle of Lamna ditropis at different cycle (that is, tail-beat) frequencies and temperatures, measured by work-loop analysis.

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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

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  1. Diego Bernal
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Correspondence to Diego Bernal or Robert E. Shadwick.

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Supplementary information

Supplementary Figure 1

In situ measures of muscle twitches. (PDF 2961 kb)

Supplementary Figure Legend

Text to accompany the above Supplementary Figure. (DOC 21 kb)

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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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