Adrenergic tone benefits cardiac performance and warming tolerance in two teleost fishes that lack a coronary circulation

Abstract

Tolerance to acute environmental warming in fish is partly governed by the functional capacity of the heart to increase systemic oxygen delivery at high temperatures. However, cardiac function typically deteriorates at high temperatures, due to declining heart rate and an impaired capacity to maintain or increase cardiac stroke volume, which in turn has been attributed to a deterioration of the electrical conductivity of cardiac tissues and/or an impaired cardiac oxygen supply. While autonomic regulation of the heart may benefit cardiac function during warming by improving myocardial oxygenation, contractility and conductivity, the role of these processes for determining whole animal thermal tolerance is not clear. This is in part because interpretations of previous pharmacological in vivo experiments in salmonids are ambiguous and were confounded by potential compensatory increases in coronary oxygen delivery to the myocardium. Here, we tested the previously advanced hypothesis that cardiac autonomic control benefits heart function and acute warming tolerance in perch (Perca fluviatilis) and roach (Rutilus rutilus); two species that lack coronary arteries and rely entirely on luminal venous oxygen supplies for cardiac oxygenation. Pharmacological blockade of β-adrenergic tone lowered the upper temperature where heart rate started to decline in both species, marking the onset of cardiac failure, and reduced the critical thermal maximum (CTmax) in perch. Cholinergic (muscarinic) blockade had no effect on these thermal tolerance indices. Our findings are consistent with the hypothesis that adrenergic stimulation improves cardiac performance during acute warming, which, at least in perch, increases acute thermal tolerance.

Whole Transcriptome Analysis of Differentially Expressed Genes in Cultured Nile Tilapia (O. niloticus) Subjected to Chronic Stress Reveals Signaling Pathways Associated with Depressed Growth

“…The growth rates were positively correlated with the relative condition factor (K n ) in both cases. This is consistent with the assertion of [ 58 ] that higher K n values are indicative of fish wellness. High SGR and K n values observed in the control fish indicate that higher growth is associated with fish wellness.…”

“…Ref. [ 58 ] demonstrated that adrenergic activation enhances heart performance in acute thermal stress in various teleost.…”

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

“…This study did not examine the mechanisms responsible for the resetting of f H , but the increase in resting f H following acclimation to 1°C could have been the result of: a shift in cardiomyocyte membrane ion channel function and/or density ( Vornanen, 1998 ; Vornanen et al, 2002a , b ); an increase in adrenoreceptor sensitivity to extrinsic factors (i.e. circulating hormones adrenaline and noradrenaline) ( Gamperl and Farrell, 2004 ); and/or a change in the cholinergic and adrenergic control of cardiac function ( Ekström et al, 2016 , 2021 ; Porter et al, 2022 ).…”

“…Average ocean temperatures are predicted to rise by 2–4°C by the end of this century ( IPCC, 2018 , 2022 ), and this has prompted in-depth research over the past several decades to understand the impacts of high water temperatures on the physiology of fish (e.g. Andreassen et al, 2022 ; Ekström et al, 2021 ; Ørsted et al, 2022 ). However, marine environments are also experiencing extreme reductions in temperatures at an increased rate, and for prolonged periods of time.…”

Hypoxic and Thermal Stress: Many Ways Leading to the NOS/NO System in the Fish Heart

“…This occurs by changing the heart rate (HR) more than the stroke volume [103,104]. When temperature acutely rises, the HR increases before declining at temperatures preceding the critical thermal maximum [103,104] and this compromises the cardiac function [102,105,106]. On the other hand, when the temperature drops, bradycardia occurs [107], and this is associated with an increased diastolic duration to maintain CO by increasing filling time and with little modifications of the systolic duration [108].…”