Can temperature-dependent changes in myocardial contractility explain why fish only increase heart rate when exposed to acute warming?

Abstract

Fish increase heart rate (fH), not stroke volume (VS), when acutely warmed as a way to increase cardiac output (Q). To assess whether aspects of myocardial function may have some basis in determining temperature-dependent cardiac performance, we measured work and power (shortening, lengthening and net) in isolated segments of steelhead trout (Oncorhynchus mykiss) ventricular muscle at the fish's acclimation temperature (14oC), and at 22oC, when subjected to increased rates of contraction (30–105 min−1, emulating increased fH) and strain amplitude (8-14%, mimicking increased VS). At 22oC, shortening power (indicative of Q) increased in proportion to fH, and the work required to re-lengthen (stretch) the myocardium (fill the heart) was largely independent of fH. In contrast, the increase in shortening power was less than proportional when strain was augmented, and lengthening work approximately doubled when strain was increased. Thus, the derived relationships between fH, strain, and myocardial shortening power and lengthening work, suggest that: increasing fH would be preferable as a mechanism to increase Q at high temperatures; or in fact, may be an unavoidable response given constraints on muscle mechanics as temperatures rise. Interestingly, at 14oC, lengthening work increased substantially at higher fHs, and the duration of lengthening (i.e., diastole) became severely constrained when fH was increased. These data suggest that myocardial contraction / twitch kinetics greatly constrain maximal fH at cool temperatures, and may underlie observations that fish elevate VS to an equal or greater extent than fH to meet demands for increased Q at lower temperatures.

Acute and chronic cold exposure differentially affect cardiac control, but not cardiorespiratory function, in resting Atlantic salmon (Salmo salar)

“…5 ). The former result is in contrast to recent data collected on myocardial strips ( Gamperl et al, 2022 ) which suggests that the effects of cool temperatures on myocardial contraction would greatly constrain f H , and that this could make increasing V S much more favourable than increasing f H to elevate at low temperatures. Given that we only assessed resting cardiorespiratory function in this study, we are planning swimming (i.e., critical swimming speed; U crit ) experiments designed to examine how acute and chronic exposure to 1 °C affect maximum values for f H , V S and .…”

“…Understanding the mechanistic basis of the latter finding will require direct measurements of these parameters in fish exposed to these temperatures, as will determining whether increases in f H and/orV S are most important for increasing in fishes at these temperatures. The recent data of Gamperl et al (2022) , based on mechanistic studies of heart function, would suggest that it is the latter. However, this hypothesis also needs experimental verification.…”

Cardiorespiratory physiology and swimming capacity of Atlantic salmon (Salmo salar) at cold temperatures

“…However, this study also reports several novel findings that have important implications for our understanding of fish temperature-dependent cardiorespiratory physiology. First, increases in f H with swimming were very limited (20–40%) in our salmon, and these data support the recent findings of Gamperl et al (2022) that suggest myocardial contraction and twitch kinetics greatly constrain maximal f H in fishes at cold temperatures. Second, while the higher resting f H in 1°C-acclimated salmon as compared with that of salmon acutely exposed to this temperature was not unexpected ( Aho and Vornanen, 2001 ; Haverinen and Vornanen, 2007 ; but also see below), the fact that these two groups used completely different mechanisms to increase blood oxygen delivery/ Ṁ O 2 when exercised ( V S and versus tissue oxygen extraction, respectively) is particularly notable.…”

“…Clearly, cold exposure regardless of duration reduced the f H,max reached when salmon were exercised to exhaustion, and we now have some insights into the underlying mechanism(s) mediating this effect. For example, Gamperl et al (2022) provide convincing data which suggests that myocardial contraction and twitch kinetics greatly constrain f H,max in rainbow trout at cool temperatures.…”

Perspective Chapter: In Vitro Contracting Cardiomyogenic Models from Whole Fish Embryos and Larvae – Method, Properties, and Applications

“…The contraction frequency of the SCCs correlated highly with temperature [29]. A steady and significant increase in their frequency with increasing temperature and vice versa was observed [29], as found in the in vivo condition in fish and mammals [37][38][39].…”