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Characterization of the functional and anatomical differences in the atrial and ventricular myocardium from three species of elasmobranch fishes: smooth dogfish (Mustelus canis), sandbar shark (Carcharhinus plumbeus), and clearnose skate (Raja eglanteria)

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Abstract

We assessed the functional properties in atrial and ventricular myocardium (using isolated cardiac strips) of smooth dogfish (Mustelus canis), clearnose skate (Raja eglanteria), and sandbar shark (Carcharhinus plumbeus) by blocking Ca2+ release from the sarcoplasmic reticulum (SR) with ryanodine and thapsigargin and measuring the resultant changes in contraction–relaxation parameters and the force–frequency relationship at 20 °C and 30 °C. We also examined ultrastructural differences with electron microscopy. In tissues from smooth dogfish, net force (per cross-sectional area) and measures of the speeds of contraction and relaxation were all higher in atrial than ventricular myocardium at both temperatures. Atrial-ventricular differences were evident in the other two species primarily in measures of the rates of contraction and relaxation. Ryanodine-thapsigargin treatment reduced net force and its maximum positive first derivative (i.e., contractility), and increased time to 50 % relaxation in atrial tissue from smooth dogfish at 30 °C. It also increased times to peak force and half relaxation in clearnose skate atrial and ventricular tissue at both temperatures, but only in atrial tissue from sandbar shark at 30 °C; indicating that SR involvement in excitation–contraction (EC) coupling is species- and temperature-specific in elasmobranch fishes, as it is in teleost fishes. Atrial and ventricular myocardium from all three species displayed a negative force–frequency relationship, but there was no evidence that SR involvement in EC coupling was influenced by heart rate. SR was evident in electron micrographs, generally located in proximity to mitochondria and intercalated discs, and to a lesser extent between the myofibrils; with mitochondria being more numerous in ventricular than atrial myocardium in all three species.

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Abbreviations

CICR:

Ca2+-induced Ca2+-release

+dF/dt max :

Maximum rate of force development (mN mm−2 s−1)

−dF/dt min :

Maximum rate of relaxation (mN mm−2 s−1)

DMSO:

Dimethyl sulfoxide

EC:

Excitation–contraction

ECG:

Electrocardiogram

G:

Glycogen storage granules

h:

Hours

Hz:

Hertz

ICD:

Intercalated discs

kHz:

Kilohertz

M:

Mitochondria

min:

Minutes

mm:

Millimeter

mN:

MilliNewtons

ms:

Millisecond

MHC:

Myosin heavy chains

NCX:

Na+–Ca2+ exchanger

nm:

Nanometers

P:

Probability

s:

Seconds

SL:

Sarcolemma

SERCA:

SR Ca2+-ATPase

SR:

Sarcoplasmic reticulum

Z:

Z-line

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Acknowledgments

The authors gratefully acknowledge Holly Shiels and Gina Galli (University of Manchester, U.K.) for their critical reviews of earlier versions of this manuscript, although any errors of omission or commission are solely ours. We also greatly recognized the entire staff of the VIMS Eastern Shore Laboratory for their ongoing hospitality and help in running the experiments. Support was provided by the Core Facility for Integrated Microscopy, University of Copenhagen; the University of Indiana South Bend; and the Northeast Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration (NOAA). This is contribution 3582 from the Virginia Institute of Marine Science, College of William and Mary. The opinions expressed herein are those of the authors and do not necessarily reflect the views of the US Department of Commerce, National Oceanic and Atmospheric Administration (NOAA), or any of their sub-agencies. Likewise, mention of trade names, products, or commercial companies is for identification purposes only and does not imply endorsement by NOAA or any of its sub-agencies. The authors declare that they have no conflicts of interest.

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Authors and Affiliations

  1. Marine Biological Section, University of Copenhagen, Strandpromenaden 5, 3000, Helsingør, Denmark

    Julie Larsen & John Steffensen

  2. Department of Biology, Indiana University South Bend, 1700 Mishawaka Avenue, South Bend, IN, 46634-7111, USA

    Peter Bushnell

  3. Department of Science and Environment, Roskilde University, Universitetsvej 1, 4000, Roskilde, Denmark

    Morten Pedersen

  4. Department of Biomedical Sciences/CFIM, University of Copenhagen, Blegdamsvej 3, 2200, Copenhagen, Denmark

    Klaus Qvortrup

  5. Behavioral Ecology Branch, Ecosystems Processes Division, Northeast Fisheries Science Center, National Marine Fisheries Service, NOAA, Sandy Hook, NJ, USA

    Richard Brill

  6. Virginia Institute of Marine Science, PO Box 1346, Gloucester Point, VA, 23062, USA

    Richard Brill

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  1. Julie Larsen
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Correspondence to Richard Brill.

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Communicated by H.V. Carey.

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Larsen, J., Bushnell, P., Steffensen, J. et al. Characterization of the functional and anatomical differences in the atrial and ventricular myocardium from three species of elasmobranch fishes: smooth dogfish (Mustelus canis), sandbar shark (Carcharhinus plumbeus), and clearnose skate (Raja eglanteria). J Comp Physiol B 187, 291–313 (2017). https://doi.org/10.1007/s00360-016-1034-9

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