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

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 that 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 that pinnipeds, which do not fluke, maintain low abdominal pressures. Simulations also showed that 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.

Contraction of atrial smooth muscle reduces cardiac output in perfused turtle hearts

“…The fact that atrial smooth muscle contraction decreases cardiac filling indicates that it may be able to constrain the rise in stroke volume during dive bradycardia. This is analogous to the contraction of the vena caval sphincter as a means to decrease stroke volume in diving mammals (Blix, 2018;Elsner et al, 1971;Harrison and Tomlinson, 1956;Lillie et al, 2018). Reducing stroke volume during diving would be energetically beneficial to the heart, as we observed smooth muscle contraction decreased cardiac power (work).…”

The Heart of the Killer Whale: Description of a Plastinated Specimen and Review of the Available Literature

“…Nevertheless, we believe the results from this study will be invaluable to clinicians, radiologists, anatomists and other research scientists interested in comparative or functional cardiac anatomy and physiology. It is imperative that comparative cardiac anatomy studies consider the implications of other systemic cardiovascular adaptations, such as of the caval sphincter in the diaphragm [52].…”

Smooth Muscle in Cardiac Chambers is Common in Turtles and Extensive in the Emydid Turtle,Trachemys scripta

“…From a functional point of view, there are least two similar adaptations to altering venous return among vertebrates. Diving mammals have a vena caval sphincter that may impede venous return during diving bradycardia (Harrison and Tomlinson, ; Elsner et al ., ; Blix, ; Lillie et al ., ) and some terrestrial snakes have a “corkscrew” caval vein that may facilitate venous return during gravitational challenges such as during climbing (Lillywhite, ; Conklin et al ., ). In consistent with earlier descriptions (Shaner, ; Robb, ), smooth muscle was sparse but consistently identified in the ventricle of T. scripta (and minute amounts were found in C. senegalensis and C. serpentina ).…”