Proceedings of The Physiological Society

Europhysiology 2018 (London, UK) (2018) Proc Physiol Soc 41, PCA022

Poster Communications

The evolution and function of atrial smooth muscle in turtles

W. Joyce1, B. Jensen2, M. Axelsson3, T. Wang1

1. Bioscience, Aarhus University, Aarhus, Denmark. 2. Medical Biology, Academic Medical Center, Amsterdam, Netherlands. 3. Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden.


By the end of the 19th century, unusual undulations in resting tension (‘tonus waves') had been repeatedly reported in atrial preparations from freshwater turtles (Emydidae). By the 1920s, these waves were married with the histological demonstration that, unlike in other animals, smooth muscle coats the luminal side of turtle atria. Since then, preciously little attention has been placed on this peculiar smooth muscle, and its evolution and physiological function remain elusive. We used fluorescent immunohistochemistry to identify smooth muscle (smooth muscle actin) and cardiac muscle (cardiac troponin I) in fixed hearts from 8 distantly related species of turtles (Chelodina mccordi (N=3), Pelodiscus sinensis (N=2), Chelydra serpentina (N=3), Pelomedusa subrufa (N=3), Cyclanorbis senegalensis (N=2), Chelonoidis carbonaria (N=3), Testudo hermanii (N=3) and Trachemys scripta (N=8)) along with reptile outgroups (two species of crocodilian (Caiman crocodilus (N=1) and Alligator mississippiensis (N=2)) and one lizard (Hemisphaeriodon gerrardii (N=1)). All animals were euthanised with an overdose of pentobarbital (200 mg kg-1) and all procedures were completed in accordance with Danish animal care legislation. Atrial smooth muscle was not detected in reptiles other than turtles (although smooth muscle was readily detected in outflow tract vasculature). Sparse atrial smooth muscle was present in atria from turtles across the phylogeny, but extensive coverage (i.e. >10% of the total tissue area on sections) was only identified in the emydid species (T. scripta). The closely related land tortoises (T. hermanii and C. carbonaria) had little atrial smooth muscle. In in situ perfused hearts (e.g. Joyce et al., 2016) of the emydid red-eared slider (T. scripta; N=6), the addition of wortmannin, which inhibits smooth muscle contraction, increased cardiac output from 24.3 ± 7.4 (mean ± S.E.M.) to 42.1 ± 5.3 ml min kg-1 (P<0.01; paired t-test). Histamine, which elicits smooth muscle contraction, stimulated a prolonged diastolic contracted state of the atria during which cardiac output was reduced from 32.6 ± 7.8 to 13.36 ± 5.8 ml min kg-1 (P<0.01; paired t-test). Extensive smooth muscle, we conclude, has evolved within turtles, where it provides a novel mechanism for the control of cardiac output. This mechanism may contribute to the tremendous diving capacity of emydid turtles.

Where applicable, experiments conform with Society ethical requirements