The caval sphincter in cetaceans and its predicted role in controlling venous flow during a dive

Author:

Lillie Margo A.1ORCID,Vogl A. Wayne2ORCID,Raverty Stephen3,Haulena Martin4,McLellan William A.5,Stenson Garry B.6ORCID,Shadwick Robert E.1ORCID

Affiliation:

1. Department of Zoology, University of British Columbia, Vancouver, B.C., V6T 1Z4, Canada

2. Department of Cellular and Physiological Sciences, University of British Columbia, Vancouver, B.C., V6T 1Z3, Canada

3. Animal Health Centre, 1767 Angus Campbell Road, Abbotsford, B.C., V3G 2M3, Canada

4. Vancouver Aquarium Marine Science Centre, PO Box 3232, Vancouver, BC, V6G 3E2, Canada

5. Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, North Carolina, USA

6. Fisheries and Oceans, Canada, St. John's, NL, A1C 5X1, Canada

Abstract

A sphincter on the inferior vena cava can protect the heart of a diving mammal from overload when elevated abdominal pressures increase venous return, yet sphincters are reported incompetent or absent in some cetacean species. We previously hypothesized that abdominal pressures are elevated and pulsatile in fluking cetaceans, and that collagen is deposited on the diaphragm according to pressure levels to resist deformation. Here we tested the hypothesis that cetaceans generating high abdominal pressures need a more robust sphincter than those generating low pressures. We examined diaphragm morphology in seven cetacean and five pinniped species. All odontocetes had morphologically similar sphincters despite large differences in collagen content, and mysticetes had muscle that could modulate caval flow. These findings do not support the hypothesis that sphincter structure correlates with abdominal pressures. To understand why a sphincter is needed, we simulated the impact of oscillating abdominal pressures on caval flow. Under low abdominal pressures, simulated flow oscillated with each downstroke. Under elevated pressures, a vascular waterfall formed, greatly smoothing flow. We hypothesize cetaceans maintain high abdominal pressures to moderate venous return and protect the heart while fluking, and use their sphincters only during low-fluking periods when abdominal pressures are low. We suggest pinnipeds, which do not fluke, maintain low abdominal pressures. Simulations also showed retrograde oscillations could be transmitted upstream from the cetacean abdomen and into the extradural veins, with potentially adverse repercussions for the cerebral circulation. We propose that locomotion-generated pressures have influenced multiple aspects of the cetacean vascular system.

Funder

Natural Sciences and Engineering Research Council of Canada

National Oceanic and Atmospheric Administration

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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