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The effects of elevated potassium, acidosis, reduced oxygen levels, and temperature on the functional properties of isolated myocardium from three elasmobranch fishes: clearnose skate (Rostroraja eglanteria), smooth dogfish (Mustelus canis), and sandbar shark (Carcharhinus plumbeus)

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Abstract

Elevated plasma potassium levels (hyperkalemia), reduced plasma pH (acidosis), reduced blood oxygen content, and elevated temperatures are associated with species-specific rates of at-vessel and post-release mortality in elasmobranch fishes. The mechanism linking these physiological disturbances to mortality remains undetermined however, and we hypothesize that the proximate cause is reduced myocardial function. We measured changes in the functional properties of isolated ventricular myocardial strips from clearnose skate (Rostroraja eglanteria), smooth dogfish (Mustelus canis), and sandbar shark (Carcharhinus plumbeus) when subjected to the following stressors (both in isolation and in combination): hyperkalemia (7.4 mM K+), acidosis (from 7.9 to 7.1), and reduced oxygen (to 31% O2 saturation) applied at temperatures 5 °C above and below holding temperatures. We selected these species based on phylogenetic distance, diverse routine activity levels, and their tolerance to capture and transport. Stressors had a few significant species-specific detrimental impacts on myocardial function (e.g., a 33–45% decrease in net force under acidosis + low O2). Net force production of myocardial strips from clearnose skate and smooth dogfish approximately doubled following exposure to isoproterenol, demonstrating that these species possess beta-adrenergic receptors and that their stimulation could provide a mechanism for preservation of cardiac function during stress. Our results suggest that disruption of physiological homeostasis associated with capture may fatally impair cardiac function in some elasmobranch species, although research with more severe stressors is needed.

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Data availability

Data is freely available through the William and Mary data repository at https://doi.org/10.25773/aamf-fb65

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Acknowledgements

We would like to thank two anonymous reviewers for their constructive comments on an earlier version of this article, T. Deemer for assistance in obtaining smooth dogfish, and D. Crear, G. Fay, and M. Winton for their assistance with statistical analysis. We would also like to thank D. Lavoie, R. Steffan, A. Sergio, T. Bigelow and the entire staff at the Virginia Institute of Marine Science Eastern Shore Laboratory for their unwavering logistical support and assistance in collecting specimens. Species silhouettes in Figs. 1-4 were provided by O. Shipley.

Funding

Support for G.S. was provided by National Science Foundation under Grant DGE‐1444317. Support for M.W. and D.B was provided by National Science Foundation under Grant IOS-1354593.

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Authors and Affiliations

  1. Department of Fisheries Science, Virginia Institute of Marine Science, William & Mary, Gloucester Point, VA, 23062, USA

    Gail D. Schwieterman & Richard W. Brill

  2. Biology Department, University of Massachusetts Dartmouth, North Dartmouth, MA, 02747, USA

    Maggie M. Winchester

  3. Faculty of Biology Medicine and Health, University of Manchester, Manchester, M13 9NT, UK

    Holly A. Shiels

  4. Department of Biology, Indiana University South Bend, South Bend, IN, 46634, USA

    Peter G. Bushnell

  5. Biology Department, University of Massachusetts Dartmouth, North Dartmouth, MA, 02747, USA

    Diego Bernal

  6. Natural Science Department, State College of Florida, Bradenton, FL, 34207, USA

    Heather M. Marshall

  7. Field Lab Consulting, Palmetto, FL, 34221, USA

    Heather M. Marshall

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  1. Gail D. Schwieterman
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  2. Maggie M. Winchester
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  3. Holly A. Shiels
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  4. Peter G. Bushnell
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  6. Heather M. Marshall
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  7. Richard W. Brill
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All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by GS and MW. The first draft of the manuscript was written by GS and MW and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Gail D. Schwieterman.

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All animal capture, care, and experimental protocols and procedures were approved by the William and Mary Institutional Animal Care and Use Committee (protocol: IACUC-2016-02-18-10947-rwbril).

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Communicated by B. Pelster.

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Supplementary Information

Below is the link to the electronic supplementary material.

Supplemental Figure 1.

The functional parameters of ventricular myocardial strips isolated from clearnose skate (a), smooth dogfish (b), and sandbar shark (c) during exposure to control conditions and hyperkalemia (7.4 mM [K+]) at two temperatures. Each line connects the same strip under exposure to the control and hyperkalemia treatments. Unpaired data points are shown to demonstrate the range of values in the raw data, but were excluded from data analysis calculated fractional changes. (TIF 49677 KB)

Supplemental Figure 2.

The functional parameters of ventricular myocardial strips isolated from clearnose skate (a), smooth dogfish (b), and sandbar shark (c) during exposure to control conditions and acidosis + low O2 at two temperatures. Each line connects the same strip under exposure to the control and hyperkalemia treatments. Unpaired data points are shown to demonstrate the range of values in the raw data, but were excluded from data analysis calculated fractional changes (TIF 23707 KB)

Supplemental Figure 3.

The functional parameters of ventricular myocardial strips isolated from clearnose skate (a), smooth dogfish (b), and sandbar shark (c) during exposure to control conditions and combined stressors (hyperkalemia, acidosis, and low O2) at two temperatures. Each line connects the same strip under exposure to the control and hyperkalemia treatments. Unpaired data points are shown to demonstrate the range of values in the raw data but were excluded from data analysis calculated fractional changes (TIF 23538 KB)

Supplemental Figure 4.

The functional parameters ventricular myocardial strips isolated from clearnose skate (a), smooth dogfish (b), and sandbar shark (c) during exposure to control conditions and isoproterenol alone (“Control + Iso) at two temperatures. Each line connects the same strip under exposure to the control and hyperkalemia treatments. Unpaired data points are shown to demonstrate the range of values in the raw data, but were excluded from data analysis calculated fractional changes (TIF 23539 KB)

Supplemental Figure 5.

The functional parameters ventricular myocardial strips isolated from clearnose skate (a), smooth dogfish (b), and sandbar shark (c) during exposure to control conditions, and to hyperkalemia, acidosis, low O2, and isoproterenol (“Combined + Iso”) at two temperatures. Each line connects the same strip under exposure to the control and hyperkalemia treatments. Unpaired data points are shown to demonstrate the range of values in the raw data, but were excluded from data analysis calculated fractional changes (TIF 23442 KB)

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Schwieterman, G.D., Winchester, M.M., Shiels, H.A. et al. The effects of elevated potassium, acidosis, reduced oxygen levels, and temperature on the functional properties of isolated myocardium from three elasmobranch fishes: clearnose skate (Rostroraja eglanteria), smooth dogfish (Mustelus canis), and sandbar shark (Carcharhinus plumbeus). J Comp Physiol B 191, 127–141 (2021). https://doi.org/10.1007/s00360-020-01328-8

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