Fish in hot water: Hypoxaemia does not trigger catecholamine mobilization during heat shock in rainbow trout (Oncorhynchus mykiss)

Currie, Suzanne; Ahmady, Elmira; Watters, Marianne; Perry, Steve F.; Gilmour, Kathleen M.

doi:10.1016/j.cbpa.2013.03.014

Cited by 28 publications

(16 citation statements)

References 38 publications

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“…Adrenergic stimulation of the heart may also be important at thermal extremes, which is consistent with increased plasma catecholamine levels observed in various teleost species during heat stress (Currie et al 2013;LeBlanc et al 2012;Forster et al 1998). Indeed, β-adrenergic stimulation improves in situ and in vitro cardiac function at elevated temperature (Gilbert et al 2019;Aho and Vornanen 2001), as well as during hypoxemia, acidosis and hyperkalemia (Farrell et al 1983;Hanson and Farrell 2007;Hanson et al 2006;Kalinin and Gesser 2002;Roberts and Syme 2018), all of which are conditions associated with increased energy turnover at elevated temperature (Cech et al 1976;Clark et al 2008b;Heath and Hughes 1973).…”

Section: Electronic Supplementary Materialssupporting

confidence: 80%

“…The supposedly impaired stroke volume and cardiac output in trout with blocked coronary blood flow likely reflected the fact that ~ 35-40% of the ventricle (based on the proportion of compact myocardium) was directly deprived of oxygen, such that cardiac aerobic metabolism was constrained, which should be exaggerated at higher temperatures as cardiac workload and oxygen demand increase (Ekström et al 2016). It should be noted, however, that we cannot exclude that the impaired cardiac performance was also partially attributed to an abolished supply of endocrine factors (e.g., catecholamines) to the compact myocardial layer, which are known to increase during warming and may benefit cardiac performance (Currie et al 2013;LeBlanc et al 2012;Forster et al 1998). Moreover, there are other less direct effects that can also explain the negative implications of blocked coronary flow on cardiac function.…”

Section: Coronary Perfusion Improves Thermal Tolerance and Cardiac Pementioning

confidence: 94%

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Can´t beat the heat? Importance of cardiac control and coronary perfusion for heat tolerance in rainbow trout

2019

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Coronary perfusion and cardiac autonomic regulation may benefit myocardial oxygen delivery and thermal performance of the teleost heart, and thus influence whole animal heat tolerance. Yet, no study has examined how coronary perfusion affects cardiac output during warming in vivo. Moreover, while β-adrenergic stimulation could protect cardiac contractility, and cholinergic decrease in heart rate may enhance myocardial oxygen diffusion at critically high temperatures, previous studies in rainbow trout (Oncorhynchus mykiss) using pharmacological antagonists to block cholinergic and β-adrenergic regulation showed contradictory results with regard to cardiac performance and heat tolerance. This could reflect intra-specific differences in the extent to which altered coronary perfusion buffered potential negative effects of the pharmacological blockade. Here, we first tested how cardiac performance and the critical thermal maximum (CT max) were affected following a coronary ligation. We then assessed how these performances were influenced by pharmacological cholinergic or β-adrenergic blockade, hypothesising that the effects of the pharmacological treatment would be more pronounced in coronary ligated trout compared to trout with intact coronaries. Coronary blockade reduced CT max by 1.5 °C, constrained stroke volume and cardiac output across temperatures, led to earlier cardiac failure and was associated with reduced blood oxygen-carrying capacity. Nonetheless, CT max and the temperatures for cardiac failure were not affected by autonomic blockade. Collectively, our data show that coronary perfusion improves heat tolerance and cardiac performance in trout, while evidence for beneficial effects of altered cardiac autonomic tone during warming remains inconclusive.

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Section: Electronic Supplementary Materialssupporting

confidence: 80%

Section: Coronary Perfusion Improves Thermal Tolerance and Cardiac Pementioning

confidence: 94%

Can´t beat the heat? Importance of cardiac control and coronary perfusion for heat tolerance in rainbow trout

2019

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“…Environmental hyperoxia in the present study was associated with a slightly lower haematocrit but not haemoglobin concentration when compared with control fish following the CT max protocol. Interestingly, a recent study on rainbow trout reported that humoral catecholamine release is reduced during thermal stress in hyperoxia (Currie et al, 2013), suggesting that the difference observed between the hyperoxic and control fish could be associated with a lower degree of adrenergic stimulation and thus red cell swelling in hyperoxic fish (Perry et al, 1996).…”

Section: Hyperoxia Increases Aerobic Scope But Not Acute Upper Thermamentioning

confidence: 99%

Experimental manipulations of tissue oxygen supply do not affect warming tolerance of European perch

Brijs

Jutfelt

Clark

et al. 2015

Journal of Experimental Biology

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A progressive inability of the cardiorespiratory system to maintain systemic oxygen supply at elevated temperatures has been suggested to reduce aerobic scope and the upper thermal limit of aquatic ectotherms. However, few studies have directly investigated the dependence of thermal limits on oxygen transport capacity. By manipulating oxygen availability (via environmental hyperoxia) and blood oxygen carrying capacity (via experimentally induced anaemia) in European perch (Perca fluviatilis Linneaus), we investigated the effects of oxygen transport capacity on aerobic scope and the critical thermal maximum (CT max ). Hyperoxia resulted in a twofold increase in aerobic scope at the control temperature of 23°C, but this did not translate to an elevated CT max in comparison with control fish (34.6± 0.1 versus 34.0±0.5°C, respectively). Anaemia (∼43% reduction in haemoglobin concentration) did not cause a reduction in aerobic scope or CT max (33.8±0.3°C) compared with control fish. Additionally, oxygen consumption rates of anaemic perch during thermal ramping increased in a similar exponential manner to that in control fish, highlighting that perch have an impressive capacity to compensate for a substantial reduction in blood oxygen carrying capacity. Taken together, these results indicate that oxygen limitation is not a universal mechanism determining the CT max of fishes.

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“…Together, they regulate the spontaneous depolarization frequency of pacemaker tissue, modifying the excitability and conductivity of atrial, ventricular and nodal tissues. Importantly, acutely warming fish greatly increases circulating catacholamines (adrenaline and noradrenaline) (Currie et al, 2013(Currie et al, , 2008, which are known to protect the performance of in situ perfused hearts, cardiac strips and isolated cardiomyocytes under a range of physiological challenges including hypoxia, acidosis, hyperkalemia and temperature (Aho and Vornanen, 2001;Farrell et al, 1996Farrell et al, , 1986Graham and Farrell, 1989;Hanson et al, 2006;Shiels et al, 2003). An elevated cardiac β-adrenergic receptor density is also associated with improved thermal tolerance in wild sockeye salmon (Eliason et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Autonomic cardiac regulation facilitates acute heat tolerance in rainbow trout:in situandin vivosupport

Gilbert

Rani

McKenzie

et al. 2019

Journal of Experimental Biology

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Acute warming in fish increases heart rate (f H) and cardiac output to peak values, after which performance plateaus or declines and arrhythmia may occur. This cardiac response can place a convective limitation on systemic oxygen delivery at high temperatures. To test the hypothesis that autonomic cardiac regulation protects cardiac performance in rainbow trout during acute warming, we investigated adrenergic and cholinergic regulation during the onset and progression of cardiac limitations. We explored the direct effects of adrenergic stimulation by acutely warming an in situ working perfused heart until arrhythmia occurred, cooling the heart to restore rhythmicity and rewarming with increasing adrenergic stimulation. Adrenergic stimulation produced a clear, dose-dependent increase in the temperature and peak f H achieved prior to the onset of arrhythmia. To examine how this adrenergic protection functions in conjunction with cholinergic vagal inhibition in vivo, rainbow trout fitted with ECG electrodes were acutely warmed in a respirometer until they lost equilibrium (CT max) with and without muscarinic (atropine) and β-adrenergic (sotalol) antagonists. Trout exhibited roughly equal and opposing cholinergic and adrenergic tone on f H that persisted up to critical temperatures. β-Adrenergic blockade significantly lowered peak f H by 14-17%, while muscarinic blockade significantly lowered the temperature for peak f H by 2.0°C. Moreover, muscarinic and β-adrenergic blockers injected individually or together significantly reduced CT max by up to 3°C, indicating for the first time that cardiac adrenergic stimulation and cholinergic inhibition can enhance acute heat tolerance in rainbow trout at the level of the heart and the whole animal.

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Fish in hot water: Hypoxaemia does not trigger catecholamine mobilization during heat shock in rainbow trout (Oncorhynchus mykiss)

Cited by 28 publications

References 38 publications

Can´t beat the heat? Importance of cardiac control and coronary perfusion for heat tolerance in rainbow trout

Can´t beat the heat? Importance of cardiac control and coronary perfusion for heat tolerance in rainbow trout

Experimental manipulations of tissue oxygen supply do not affect warming tolerance of European perch

Autonomic cardiac regulation facilitates acute heat tolerance in rainbow trout:in situandin vivosupport

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