How the efficiency of rainbow trout (Oncorhynchus mykiss) ventricular muscle changes with cycle frequency

Abstract

SUMMARYDifferent species of animals require different cardiac performance and, in turn, their cardiac muscle exhibits different properties. A comparative approach can reveal a great deal about the mechanisms underlying myocardial contraction. Differences in myocardial Ca2+ handling between fish and mammals suggest a greater energy cost of activation in fish. Further, while there is considerable evidence that heart rate (or cycle frequency) should have a profound effect on the efficiency of teleost cardiac muscle, this effect has been largely overlooked. We set out to determine how cycle frequency affects the power output and efficiency of rainbow trout (Oncorhynchus mykiss) ventricular muscle and to relate this to the heart’s function in life. We measured power output and the rate of oxygen consumption (V̇O2) and then calculated efficiency over a physiologically realistic range of cycle frequencies.In contrast to mammalian cardiac muscle, in which V̇O2 increases with increasing heart rate, we found no significant change in V̇O2 in the teleost. However, power output increased by 25 % as cycle frequency was increased from 0.6 to 1.0 Hz, so net and total efficiency increased. A maximum total efficiency of 20 % was achieved at 0.8 Hz, whereas maximum power output occurred at 1.0 Hz. We propose that, since the heart operates continuously, high mechanical efficiency is a major adaptive advantage, particularly at lower heart rates corresponding to the more commonly used slower, sustainable swimming speeds. Efficiency was lower at the higher heart rates required during very fast swimming, which are used during escape or prey capture.If a fixed amount of Ca2+ is released and then resequestered each time the muscle is activated, the activation cost should increase with frequency. We had anticipated that this would have a large effect on the total energy cost of contraction. However, since V̇O2 remains constant, less oxygen is consumed per cycle at high frequencies. We suggest that a constant V̇O2 would be observed if the amount of activator Ca2+ were to decrease with frequency. This decrease in activation energy is consistent with the decrease in the systolic intracellular Ca2+ ([Ca2+]i) transient with increasing stimulation frequency seen in earlier studies.