S ome fishes including salmonids have a coronary circulation that supplies the outer compact myocardium of the heart with fully oxygenated blood. This arterial blood supply complements the luminal venous O2 supply that delivers relatively poorly oxygenated blood to the inner spongy myocardium. T he role of the coronary circulation may be of particular relevance in farmed salmonid fishes , as our group (and others) have shown that they more frequently develop lesions and arteriosclerosis in the main coronary artery ; a condition that narrows the vessel lumen and may decrease blood flow to the myocardium (Brijs et al, 2020; Farrell, 2002). This condition can , in turn, reduce overall cardiac and metabolic performance, and possibly the tolerance to environmental stressors that incur an elevated metabolic challenge . There is also a growing body of evidence demonstrating that coronary lesion development is positively correlated with factors promoting rapid growth in the smolt production phase (e.g., supra-optimal rearing temperatures ; Brijs et al, 2020), and may be a key factor underlying adult fish mortality in aquaculture (Poppe et al , 2021) . Yet, it is still not fully understood how coronary blood flow affects overall cardiorespiratory performance. Moreover, its functional role in setting tolerance limits to environmental extremes such as heat waves and hypoxia, and how it affects resilience to stressful metabolic challenges in aquaculture, has not been extensively studied . Thus, to analyze the functional significance of coronary oxygen delivery in salmonids , we measured in vivo coronary blood flow under various thermal regime s in male and female rainbow trout (Ekström et al, 2017) . In an additional series of experiments, we surgically ligated the coronary artery to mimic extreme coronary arteriosclerosis and explored its impact on cardiovascular performance and metabolic scope (Ekström et al, 2017; Morgenroth et al, 2021), a s well as hypoxia and warming tolerance limits (Ekström et al , 2019; Morgenroth et al, 2021).
Material and methods
F ish were anesthetized in aerated freshwater (10°C) containing buffered MS-222. In one experiment, t he coronary artery was dissected free and a Transonic transit time blood flow probe was placed around the vessel. In other experiments , the vessel was exposed and either ligated with a silk suture or left intact resulting in surgically ligated and sham operated experimental groups, respectively. In some experiments, sham and ligated fish were additionally instrumented with a flow probe around the ventral aorta to measure cardiac output or custom-made subcutaneous electrodes to record the electrocardiogram (ECG) and heart rate. Fish were typically left to recover from surgery for 24-48 h in respirometers to record oxygen consumption rate and then exposed to various metabolic and environmental challenges including exhaustive exercise , acute warming and aquatic hypoxia.
Results and Discussion
Routine coronary blood flow at 10°C was markedly higher in females than males (0.56±0.08 vs. 0.30±0.08 ml min-1 g-1 ventricle). Warming increased coronary blood flow in both sexes until 14°C, at which it peaked and plateaued. This meant that the scope for increasing coronary blood flow during warming was 101% in males, but only 39% in females. While coronary ligation reduced routine stroke volume relative to sham operated trout with intact coronaries, cardiac output and standard metabolic rate was maintained via an increase in heart rate. However, coronary ligated trout had reduced maximum oxygen consumption rate and aerobic scope when subjected to a 5 min exhaustive exercise protocol , and they had a markedly reduced ability to increase stroke volume to maintain cardiac output when bradycardia developed during acute hypoxia exposure. This was associated with a slightly reduced hypoxia tolerance in coronary ligated trout . During acute warming, coronary ligation caused cardiac function to collapse at lower temperatures and significantly reduced the overall acute warming tolerance relative to sham operated trout with intact coronaries.
Collectively, our findings show that coronary perfusion improves cardiac O2 supply and overall cardiorespiratory function at environmental extremes, which benefits tolerance to environmental and anthropogenic metabolic challenges. The aquaculture industry should, therefore, consider the potentially detrimental effects of rapid smolt growth rate on coronary health and functionality , as this may result in raising fish that are more susceptible to environmental and metabolic stressors in challenging farm environment s. In light of these findings , we are currently conducting several new experiments to shed light on how juvenile rearing conditions subsequently impact cardiac and coronary health of the adult fish .