Temperature effects on the contractile performance and efficiency of oxidative muscle from a eurythermal versus a stenothermal salmonid

Abstract

We compared the thermal sensitivity of oxidative muscle function between the eurythermal Atlantic salmon (Salmo salar) and the more stenothermal Arctic char (Salvelinus alpinus; which prefers cooler waters). Power output was measured in red skeletal muscle strips and myocardial trabeculae, and efficiency (net work/energy consumed) was measured for trabeculae, from cold (6oC) and warm (15oC) acclimated fish at temperatures from 2-26oC. The mass-specific net power produced by char red muscle was greater than in salmon, by 2-5 fold depending on test temperature. Net power first increased, then decreased, when the red muscle of 6oC-acclimated char was exposed to increasing temperature. Acclimation to 15oC significantly impaired mass-specific power in char (by ∼40-50%) from 2 to 15oC, but lessened its relative decrease between 15 and 26oC. In contrast, maximal net power increased, and then plateaued, with increasing temperature in salmon from both acclimation groups. Increasing test temperature resulted in a ∼3-5 fold increase in maximal net power produced by ventricular trabeculae in all groups, and this effect was not influenced by acclimation temperature. Nonetheless, lengthening power was higher in trabeculae from warm acclimated char, and char trabeculae could not contract as fast as those from salmon. Finally, the efficiency of myocardial net work was approximately 2-fold greater in 15oC acclimated salmon than char (∼15 vs. 7%), and highest at 20oC in salmon. This study provides several mechanistic explanations as to their inter-specific difference in upper thermal tolerance, and potentially why southern char populations are being negatively impacted by climate change.

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

“…However, this species is capable of metabolic depression at low temperatures ( Costa et al, 2013 ; Gerber et al in final prep), and thus, the results of this research are unlikely to be representative of most teleosts. Data on temperature dependent changes collected using in situ or in vitro preparations are limited (e.g., Aho and Vornanen, 2001 ; Gamperl and Syme, 2021 ; Lurman et al, 2012 ), and may not accurately reflect temperature-dependent responses in in vivo cardiac performance. Finally, other literature on this topic is largely restricted to: the investigation of cardiac remodelling (including changes in relative ventricular mass; RVM) ( Aho and Vornanen, 2001 ; Driedzic et al, 1996 ; Eliason and Anttila, 2017 ; Johnson et al, 2014 ; Keen et al, 2017 ; Klaiman et al, 2011 ); or to experiments where anaesthetized fish were given pharmacological agents (atropine and isoproterenol) and exposed to very rapid acute changes in temperature so that their ‘maximum’ heart rate and its Arrhenius breakpoint at high temperatures could be measured (e.g., see Gilbert et al, 2020 ; Gilbert and Farrell, 2021 ).…”

“…However, chronic exposure to cold (∼0–1 °C) temperatures during the winter months, as well as acute daily drops in temperature (to < 2 °C) due to ‘turn over’ caused by rough conditions, are associated with large-scale mortalities at salmon sea-cages in these countries ( Círíc, 2020 ; CBC News, 2020 ; Huffman, 2019 ; The Canadian Press, 2015 ). Our understanding of how warm (summer) temperatures affect cultured Atlantic salmon has improved greatly over the past few years ( Anttila et al, 2014 ; Beemelmanns et al, 2020 , 2021 ; Gamperl et al, 2020 ; Gamperl and Syme, 2021 ; Hvas et al, 2017 ; Penney et al, 2014 ; Tromp et al, 2018 ). However, we have a very limited understanding of how the biology and physiology of this species is affected by short-term and long-term exposure to cold temperatures, and the results of this research can be contradictory (e.g., see Liu et al, 2020 vs. Sandnes et al, 1988 ).…”

Acute Toxicity of Household-Scale Lebak Batik Industrial Wastewater on Common Carp

“…Based on previous research, a temperature of 20-28 o C had a good survival rate of common carp that was 100%. Still, the best growth was at a temperature of 28 o C with an increase in absolute length and absolute weight of 2.59 cm and 4.38 g, respectively (Gamperl & Syme, 2021;Ridwantara dkk., 2019). At the same time, the pH of the results of this study can be said to be good.…”

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

“…For example, it is typically reported that red muscle mass and fibre size (diameter) increase, the oxidative capacity of red muscle is greater, and cold acclimation results in changes in muscle mechanics that enable the muscle to produce more power ( Egginton and Cordiner, 1997 ; Egginton and Sidell, 1989 ; Guderley, 2004 ; Johnston et al, 1990 ; Jones and Sidell, 1982 ; Rome and Swank, 2001 ). Further, and importantly, Gamperl and Syme (2021) reported that the red muscle of 6°C-acclimated Atlantic salmon was able to produce more power when tested at 2°C than that of 15°C-acclimated fish.…”

“… Gamperl and Syme (2021) recently published data that strongly suggest that myocardial contraction/twitch kinetics greatly constrain maximal heart rate ( f H,max ) at cool or cold temperatures, and that this may require fish to elevate stroke volume ( V S ) to an equal or greater extent than f H to meet demands for increased cardiac output ( ). To test this hypothesis, and to examine how long- and short-term changes in temperature near the lower limits for this species affect cardiac function, metabolic physiology, blood oxygen carrying capacity and swimming performance, we acclimated Atlantic salmon to 8, 4 and 1°C, and exposed a group of 8°C-acclimated fish to an acute drop in temperature to 1°C.…”