Adaptations to deep and prolonged diving in phocid seals

Journal of Experimental Biology

Axelsson

Wang

2019

Unusual undulations in resting tension (tonus waves) were described in isolated atria from freshwater turtles more than a century ago. These tonus waves were soon after married with the histological demonstration of a rich layer of smooth muscle on the luminal side of the atrial wall. Research thereafter waned and the functional significance of this smooth muscle has remained obscure. Here, we provide evidence that contraction of the smooth muscle in the atria may be able to change cardiac output in turtle hearts. In in situ perfused hearts of the red-eared slider turtle (Trachemys scripta elegans), we demonstrated that activation of smooth muscle contraction with histamine (100 nmol kg −1 bolus injected into perfusate) reduced cardiac output by decreasing stroke volume (>50% decrease in both parameters). Conversely, inhibition of smooth muscle contraction with wortmannin (10 µmol l −1 perfusion) approximately doubled baseline stroke volume and cardiac output. We suggest that atrial smooth muscle provides a unique mechanism to control cardiac filling that could be involved in the regulation of stroke volume during diving.

Section: Discussionmentioning

confidence: 53%

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

Journal of Experimental Biology

Axelsson

Wang

2019

“…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 ).…”

Section: Discussionmentioning

confidence: 99%

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

Crossley

Wang

et al. 2019

The Anatomical Record

A prominent layer of smooth muscle lining the luminal side of the atria of freshwater turtles (Emydidae) was described more than a century ago. We recently demonstrated that this smooth muscle provides a previously unrecognized mechanism to change cardiac output in the emydid red-eared slider (Trachemys scripta) that possibly contributes to their tremendous diving capacity. The purpose of the present immunohistochemical study was firstly to screen major groups of vertebrates for the presence of cardiac smooth muscle. Secondly, we investigated the phylogenetic distribution of cardiac smooth muscle within the turtle order (Testudines), including terrestrial and aquatic species. Atrial smooth muscle was not detected in a range of vertebrates, including Xenopus laevis, Alligator mississippiensis, and Caiman crocodilus, all of which have pronounced diving capacities. However, we confirmed earlier reports that traces of smooth muscle are found in human atrial tissue. Only within the turtles (eight species) was there substantial amounts of nonvascular smooth muscle in the heart. This amount was greatest in the atria, while the amount in proportion to cardiac muscle was greater in the sinus venosus than in other chambers. T. scripta had more smooth muscle in the sinus venosus and atria than the other turtles. In some specimens, there was some smooth muscle in the ventricle and the pulmonary vein. Our study demonstrates that cardiac smooth muscle likely appeared early in turtle evolution and has become extensive within the Emydidae family, possibly in association with diving. Across other tetrapod clades, cardiac smooth muscle might not associate with diving.

“…By conventionor at least without explicit justificationresistance has typically been favoured amongst comparative cardiovascular physiologists (e.g. Altimiras and Axelsson, 2004;Axelsson et al, 1992;Blix, 2018;Crossley et al, 1998;Ekström et al, 2016;Gamperl et al, 2011;Keen et al, 2016;Mendonça and Gamperl, 2009;Sandblom et al, 2005). However, it has long been recognised within the mammalian (i.e.…”

Section: Introductionmentioning

confidence: 99%

Weighing the evidence for using vascular conductance, not resistance, in comparative cardiovascular physiology

Journal of Experimental Biology

White

Raven

et al. 2019

Vascular resistance and conductance are reciprocal indices of vascular tone that are often assumed to be interchangeable. However, in most animals in vivo, blood flow (i.e. cardiac output) typically varies much more than arterial blood pressure. When blood flow changes at a constant pressure, the relationship between conductance and blood flow is linear, whereas the relationship between resistance and blood flow is non-linear. Thus, for a given change in blood flow, the change in resistance depends on the starting point, whereas the attendant change in conductance is proportional to the change in blood flow regardless of the starting conditions. By comparing the effects of physical activity at different temperatures or between speciesconcepts at the heart of comparative cardiovascular physiologywe demonstrate that the difference between choosing resistance or conductance can be marked. We also explain here how the ratio of conductance in the pulmonary and systemic circulations provides a more intuitive description of cardiac shunt patterns in the reptilian cardiovascular system than the more commonly used ratio of resistance. Finally, we posit that, although the decision to use conductance or resistance should be made on a case-by-case basis, in most circumstances, conductance is a more faithful portrayal of cardiovascular regulation in vertebrates.