Thermal effects on red muscle contractile performance in deep-diving, large-bodied fishes

Abstract

Bigeye thresher sharks (Alopias superciliosus) and swordfish (Xiphias gladius) are large, pelagic fishes, which make long-duration, diurnal foraging dives from warm, surface waters (18–24 °C) to cold waters beneath the thermocline (5–10 °C). In bigeye thresher sharks, the subcutaneous position of the red, aerobic swimming muscles (RM) suggests that RM temperature mirrors ambient during dives (i.e., ectothermy). In swordfish, the RM is closer to the vertebrae and its associated with vascular counter-current heat exchangers that maintain RM temperature above ambient (i.e., RM endothermy). Here, we sought to determine how exposure to a wide range of ambient temperatures (8, 16, 24 °C) impacted peak power output and optimum cycle (i.e., tailbeat) frequency (0.25, 0.5, 1 Hz) in RM isolated from both species. Bigeye thresher shark RM did not produce substantial power at high cycle frequencies, even at high temperatures; but it did produce relatively high power at slow cycle frequencies regardless of temperature. Swordfish RM produced more power when operating at a combination of fast cycle frequencies and higher temperatures. This suggests that swordfish RM benefits considerably more from warming than bigeye thresher shark RM, while the RM of both species was able to produce power at cold temperatures and slow cycle frequencies. Despite different thermal strategies (i.e., ectothermy vs. RM endothermy), the ability of the RM to power sustained swimming during foraging-related search behaviors may contribute to the unique ability of these fishes to successfully exploit food resources in deep, cold water.

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Acknowledgments

We express our gratitude for the support of Darryl Lewis and the Harris Foundation and the continued dedication of Mr. Thomas Pfleger and Family. Individuals who assisted in this work include Cpt. Thomas “Cowboy” Fullam, Craig Heberer, Paul Tutunjian, Drew White, Ralph Pace, Jennifer Thirkell, and many commercial fisherman, especially, Donald Krebs, and Kelly Fukushima.

Funding

This material is based on the work supported by the National Science Foundation under grants IOS-1354593 and 1354772. Support for A.S. was through the University of Massachusetts Distinguished Doctoral Fellowship, National Science and Engineering Graduate Fellowship, and Sigma Xi Grant-in-Aid-of-Research.

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figure5

Stimulus parameters maximizing net-work at a given temperature and cycle frequency for a bigeye thresher sharks and b swordfish. Bar graphs depict the absolute time (ms) of a given strain cycle (0.25–1 Hz), while dashed lines demarcating the initial lengthening and shortening periods. Shaded regions display the onset and duration of stimulation expressed in time (ms) relative to the strain cycle. Optimum cycle frequencies for each temperature are denoted by an “O” symbol. In all cases optimum stimulation occurred during the initial lengthening period, resulting in an inverse relationship between optimum stimulus phase and duration with optimum cycle frequency, as faster cycle frequencies necessitated earlier and shorter stimulation periods to ensure stimulation proceeded shortening and encompassed 10–20% of strain cycle. This stimulation pattern has been shown enhance force production in vertebrate muscle by permitting optimal positioning of the contractile machinery (i.e. cross-bridge attachment) and greater activation during the shortening phase (Josephson 1993). Averages for optimum stimulus phase were 7.54 ± 0.70 for bigeye thresher sharks and 6.90 ± 0.76 for swordfish. Averages for optimum stimulus duration were 384 ± 18 ms in bigeye thresher sharks and 296 ± 20 ms in swordfish (PNG 64 kb)

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Stoehr, A.A., Donley, J.M., Aalbers, S.A. et al. Thermal effects on red muscle contractile performance in deep-diving, large-bodied fishes. Fish Physiol Biochem (2020). https://doi.org/10.1007/s10695-020-00831-7

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Keywords

  • Highly migratory fishes
  • Red muscle
  • Temperature
  • Contractile mechanics
  • Work loop
  • Swordfish
  • Bigeye thresher shark