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The functional significance and evolution of the coronary circulation in sharks Cox, Georgina Kimberly

Abstract

The coronary circulation first appeared in the chordate lineage in cartilaginous fishes where it perfuses the entire myocardium, just like in birds and mammals but unlike in most teleost fishes. Yet, despite the pivotal position of elasmobranchs in the evolution of the coronary oxygen supply, the functional significance of their coronary circulation has never been investigated. Elasmobranchs are of special interest because of the morphological arrangement of their cardiomyocytes, which has resulted in the majority of the ventricular myocardium having access to oxygen from both a coronary supply and the venous blood returning to the heart. In order to determine the relative contribution of the coronary oxygen supply to cardiovascular function, I measured coronary blood flow (CBF) in the sandbar shark, Carcharhinus plumbeus, and leopard shark, Triakis semifasciata, while manipulating cardiovascular status using pharmacological approaches and in vivo temperature changes, respectively. By exploring inter- and intra-individual variation in cardiovascular variables I show that coronary blood flow is directly related to heart rate in both bradycardic (R²= 0.6, P <0.001) and trachycardic (R²= 0.8, P <0.001) states, as it is in mammalian hearts. I suggest that changes in heart rate are related to changes in coronary vascular resistance in elasmobranchs. As I found that 3-4% of cardiac output is directed towards the myocardium (~0.07% of body mass), a methodology was developed to quantify the degree of the coronary vascularization within the spongy and compact tissues of the shark myocardium. Using this methodology, coronary vascularity and vessel morphology of six species of shark were compared to explore the functional relationships between coronary morphology and physiological phenotypes across species. I further determined that the coronary circulation showed evidence of having evolved in response to different thermal regimes across species. Together the results of this thesis show that the coronary circulation in sharks plays a crucial role in myocardial oxygen delivery to the entire heart, something not previously appreciated, and that habitat temperature plays a role as a selective agent in shaping coronary morphology.

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Attribution-NonCommercial-NoDerivs 2.5 Canada