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First published online May 8, 2007
Journal of Experimental Biology 210, 1715-1725 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02781

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Review Article

Tribute to P. L. Lutz: a message from the heart – why hypoxic bradycardia in fishes?

A. P. Farrell

Zoology Department, 6270 University Boulevard, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

e-mail: farrellt{at}interchange.ubc.ca

Accepted 19 March 2007

The sensing and processing of hypoxic signals, the responses to these signals and the modulation of these responses by other physical and physiological factors are an immense topic filled with numerous novel and exciting discoveries. Nestled among these discoveries, and in contrast to mammals, is the unusual cardiac response of many fish to environmental hypoxia – a reflex slowing of heart rate. The afferent and efferent arms of this reflex have been characterised, but the benefits of the hypoxic bradycardia remain enigmatic since equivocal results have emerged from experiments examining the benefit to oxygen transfer across the gills. The main thesis developed here is that hypoxic bradycardia could afford a number of direct benefits to the fish heart, largely because the oxygen supply to the spongy myocardium is precarious (i.e. it is determined primarily by the partial pressure of oxygen in venous blood, Pv_O2) and, secondarily, because the fish heart has an unusual ability to produce large increases in cardiac stroke volume (V_SH) that allow cardiac output to be maintained during hypoxic bradycardia. Among the putative benefits of hypoxic bradycardia is an increase in the diastolic residence time of blood in the lumen of the heart, which offers an advantage of increased time for diffusion, and improved cardiac contractility through the negative force–frequency effect. The increase in V_SH will stretch the cardiac chambers, potentially reducing the diffusion distance for oxygen. Hypoxic bradycardia could also reduce cardiac oxygen demand by reducing cardiac dP/dt and cardiac power output, something that could be masked at cold temperature because of a reduced myocardial work load. While the presence of a coronary circulation in certain fishes decreases the reliance of the heart on Pv_O2, hypoxic bradycardia could still benefit oxygen delivery via an extended diastolic period during which peak coronary blood flow occurs. The notable absence of hypoxic bradycardia among fishes that breathe air during aquatic hypoxia and thereby raise their Pv_O2, opens the possibility that that the evolutionary loss of hypoxic bradycardia may have coincided with some forms of air breathing in fishes. Experiments are needed to test some of these possibilities. Ultimately, any potential benefit of hypoxic bradycardia must be placed in the proper context of myocardial oxygen supply and demand, and must consider the ability of the fish heart to support its routine cardiac power output through glycolysis.

Key words: heart rate, stroke volume, myocardial hypoxia, oxygen diffusion, coronary circulation, air breathing

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