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

Abstract

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.

What determines systemic blood flow in vertebrates?

“…The classical studies established that vagal stimulation is a powerful stimulator of atrial smooth muscle contraction (Bottazzi, 1900;Fano and Fayod, 1888;Meek, 1927), suggesting that it probably co-occurs with the dive bradycardia, which is also vagally mediated (Burggren, 1975). Atrial smooth muscle is generally more prevalent in aquatic than in terrestrial species of turtle (Joyce et al, 2019d), further supporting the idea that it is involved in the regulation of cardiac output during diving.…”

Anatomy of the heart with the highest heart rate

“…Whales have a sphincter at the same position (Lillie et al, 2018 ), but not a valve of leaflets. Even in reptiles, where the caval vein myocardium functions as a chamber and a valve in the CCV would seem advantageous (Jensen et al, 2017 ; Joyce et al, 2020 ), there is no valve. Because such valve is rarely sought after and it may easily be obscured by coagulated blood or by its collapse against the vessel wall, a dedicated investigation may be required to establish whether a valve in the CCV is highly unusual among vertebrates.…”

Low incidence of atrial septal defects in nonmammalian vertebrates

“…We made use of previously published sections for hearts of adult birds (Kroneman et al, 2019 ), adult Anolis carolinensis (Jensen, Moorman, & Wang, 2014 ), adult Python regius (Jensen et al, 2017 ), and hearts of developing Pantherophis guttatus and Norops sagrei (B. Jensen et al, 2013 ) and Varanus indicus and Varanus acanthurus (Hanemaaijer et al, 2019 ). From (Joyce et al, 2019 ) we made use of sections of the following species: ( Pelomedusa subrufa ( n = 3; 20–35 g), Chelodina mccordi ( n = 3; 14–15 g), Pelodiscus sinensis ( n = 2; 5 g), Cyclanorbis senegalensis ( n = 2; 0.2–0.45 kg), Testudo hermanii ( n = 3; 25–27 g), Chelonoidis carbonaria ( n = 3; 2.4–4.8 kg), Chelydra serpentina ( n = 3; 30–35 g), and Trachemys scripta ( n = 10; 0.3–1.7 kg), a skink, Cyclodomorphus gerrardii , ( n = 1; 0.44 kg), an Alligator mississippiensis ( n = 1; 2 kg), a spectacled caiman, Caiman crocodilus ( n = 1; 4 kg), African clawed frogs ( Xenopus laevis ; n = 2; 50 g), and cane toads ( Rhinella marinus ; n = 2; 100–200 g). Fertilized surplus eggs of Siamese crocodile ( Crocodylus siamensis ) were obtained from The Crocodile Zoo Protivin between years 2013 and 2018 (5 embryos).…”