Coronary blood flow influences tolerance to environmental extremes in fish

Abstract

Approximately half of all fishes have, in addition to the luminal venous O2 supply, a coronary circulation supplying the heart with fully oxygenated blood. Yet, it is not fully understood how coronary O2 delivery affects tolerance to environmental extremes such as warming and hypoxia. Hypoxia reduces arterial oxygenation, while warming increases overall tissue O2 demand. Thus, as both stressors are associated with reduced venous O2 supply to the heart, we hypothesised that coronary flow benefits hypoxia and warming tolerance. To test this hypothesis, we blocked coronary blood flow (via surgical coronary ligation) in rainbow trout (Oncorhynchus mykiss), and assessed how in vivo cardiorespiratory performance and whole-animal tolerance to acute hypoxia and warming was affected. While coronary ligation reduced routine stroke volume relative to trout with intact coronaries, cardiac output was maintained by increases in heart rate. However, in hypoxia, coronary ligated trout were unable to increase stroke volume to maintain cardiac output when bradycardia developed, which was associated with a slightly reduced hypoxia tolerance. Moreover, during acute warming coronary ligation caused cardiac function to collapse at lower temperatures, and reduced overall heat tolerance relative to trout with intact coronaries. We also found a positive relationship between individual hypoxia and heat tolerance across treatment groups, and tolerance to both environmental stressors was positively correlated with cardiac performance. Collectively, our findings show that coronary perfusion improves cardiac O2 supply, and therefore, cardiovascular function at environmental extremes, which benefits tolerance to natural and anthropogenically induced environmental perturbations.

Adaptation of a mouse Doppler echocardiograph system for assessing cardiac function and thermal performance in a juvenile salmonid

“…We used ventricular inflow volume as a proxy for stroke volume, assuming low variation in ejection fraction between heartbeats at a given temperature. Indeed, the ventricular inflow volumes reported here (mean of 0.43 ± 0.04 ml kg −1 at maximum; Table 1 ) are comparable to stroke volumes reported in other salmonid species (0.2–1.2 ml kg −1 ; Clark et al , 2008 ; Steinhausen et al , 2008 ; Eliason et al , 2013 ; Morgenroth et al , 2021 ). By measuring f Hmax simultaneously with this proxy for stroke volume, this system allowed for calculations of extrapolated cardiac output across a range of experimental temperatures.…”

“…By measuring f Hmax simultaneously with this proxy for stroke volume, this system allowed for calculations of extrapolated cardiac output across a range of experimental temperatures. Estimations of peak cardiac output made here (mean of 42.2 ml min −1 kg −1 ; Table 1 ) fall within the range of peak cardiac output values obtained in salmonids fitted with transonic blood flow probes (17–110 ml min −1 kg −1 ; Clark et al , 2008 ; Steinhausen et al , 2008 ; Eliason et al , 2013 ; Ekström et al , 2017 ; Morgenroth et al , 2021 ). While these internal flow probes are commonly used to measure cardiac output in fish, test fish must be large enough for the equipment to be properly placed and supported for the duration of the experiment ( Eliason et al , 2013 ).…”

“…Interestingly, declines in stroke distance began to plateau at temperatures beyond the T AB for f Hmax , when the rate at which f Hmax increases with temperature slows. Similar patterns in heart rate and stroke volume were demonstrated in unanaesthetized rainbow trout ( Oncorhynchus mykiss ) fitted with internal blood flow probes during determinations of CT max ( Morgenroth et al , 2021 ). Our findings demonstrate the utility of this system as a nonsurgical method for estimating changes in cardiac output and investigating force-frequency dynamics across a range of experimental temperatures.…”

High temperature impairs mitochondrial function in rainbow trout cardiac mitochondria

“…Our results contribute to previous work on the influence of mitochondrial function on thermal tolerance, and suggest that proper function of heart mitochondria is more critical in determining the thermal tolerance of fish compared with liver mitochondria, which most of the previous work is based on (Chung and Schulte, 2020), consistent with the general view that the heart may be one of the first organs to be limited by heat stress (Clark et al, 2008;Eliason et al, 2011;Pörtner and Farrell, 2008). Alternatively, the rainbow trout might be an exception to the general rule, as oxygen delivery to the heart is not a limiting factor with heat stress in this species (Motyka et al, 2017), due at least in part to the coronary circulation (Ekström et al, 2019;Morgenroth et al, 2021). Finally, our study, along with others (Birkedal and Gesser, 2003;Christen et al, 2018;Iftikar et al, 2014) indicates that some specific properties of mitochondrial function, in particular the phosphorylation system, appear more sensitive to heat stress than oxygen consumption by the ETC per se.…”

“…The rainbow trout (Oncorhynchus mykiss) is a cold-water stenotherm with an upper thermal limit between 27 and 32°C, depending on acclimation temperature (Chen et al, 2015;Currie et al, 1998), and a peak in aerobic scope at around 20°C (Chen et al, 2015). Trout is an example of a species that is not limited by oxygen delivery to the heart at high temperatures (Motyka et al, 2017), at least in part due to the presence of coronary arteries supplying the heart with welloxygenated blood (Ekström et al, 2019;Morgenroth et al, 2021). Thus, this species allows disentangling contributions from limitations in oxygen supply to the heart and oxygen consumption by the cardiac mitochondria in determining the thermal tolerance of this species.…”