journal article Open Access Feb 15, 2022

Can temperature-dependent changes in myocardial contractility explain why fish only increase heart rate when exposed to acute warming?

View at Publisher Save 10.1242/jeb.243152
Abstract
ABSTRACT
Fish increase heart rate (fH), not stroke volume (VS), when acutely warmed as a way to increase cardiac output (Q). To assess whether aspects of myocardial function may have some basis in determining temperature-dependent cardiac performance, we measured work and power (shortening, lengthening and net) in isolated segments of steelhead trout (Oncorhynchus mykiss) ventricular muscle at the fish's acclimation temperature (14°C), and at 22°C, when subjected to increased rates of contraction (30–105 min−1, emulating increased fH) and strain amplitude (8–14%, mimicking increased VS). At 22°C, shortening power (indicative of Q) increased in proportion to fH, and the work required to re-lengthen (stretch) the myocardium (fill the heart) was largely independent of fH. In contrast, the increase in shortening power was less than proportional when strain was augmented, and lengthening work approximately doubled when strain was increased. Thus, the derived relationships between fH, strain and myocardial shortening power and lengthening work, suggest that increasing fH would be preferable as a mechanism to increase Q at high temperatures, or in fact may be an unavoidable response given constraints on muscle mechanics as temperatures rise. Interestingly, at 14°C, lengthening work increased substantially at higher fH, and the duration of lengthening (i.e. diastole) became severely constrained when fH was increased. These data suggest that myocardial contraction/twitch kinetics greatly constrain maximal fH at cool temperatures, and may underlie observations that fish elevate VS to an equal or greater extent than fH to meet demands for increased Q at lower temperatures.
Topics

No keywords indexed for this article. Browse by subject →

References
46
[1]
Altringham "Scaling effects on muscle function: power output of isolated fish muscle fibres performing oscillatory work" J. Exp. Biol. (1990) 10.1242/jeb.151.1.453
[2]
Andreassen "Neural dysfunction at the upper thermal limit in the zebrafish" (2020) 10.1101/2020.12.28.424529
[3]
Ask "Temperature effects on the β-adrenoreceptors of the trout atrium" J. Comp. Physiol. (1981) 10.1007/bf00797695
[4]
Bijnens "Myocardial motion and deformation: what does it tell us and how does it relate to function?" Fetal Diagn. Ther. (2012) 10.1159/000335649
[5]
Brett "The relation of size to rate of oxygen consumption and sustained swimming speed of Sockeye salmon (Oncorhynchus nerka)" J. Fish. Res. Board Can. (1965) 10.1139/f65-128
[6]
Carnevale, C. (2019). The effects of chronic hypoxia and nitric oxide on myocardial contractility in steelhead trout (Oncorhynchus mykiss). MSc Thesis, Memorial University of Newfoundland, St. John's. https://research.library.mun.ca/14317/1/thesis.pdf.
[7]
Carnevale "Effects of hypoxic acclimation, muscle strain, and contraction frequency on nitric oxide-mediated myocardial performance in steelhead trout (Oncorhynchus mykiss)" Am. J. Physiol. Regul. Integr. Comp. Physiol. (2021) 10.1152/ajpregu.00014.2020
[8]
Marine heatwaves exacerbate climate change impacts for fisheries in the northeast Pacific

William W. L. Cheung, Thomas L. Frölicher

Scientific Reports 2020 10.1038/s41598-020-63650-z
[9]
Christen "Thermal tolerance and thermal sensitivity of heart mitochondria: Mitochondrial integrity and ROS production" Free Radic. Biol. Med. (2018) 10.1016/j.freeradbiomed.2017.12.037
[10]
Eliason "Temperature and the cardiovascular system" (2017)
[11]
Farrell "Environment, antecedents and climate change: lessons from the study of temperature physiology and river migration of salmonids" J. Exp. Biol. (2009) 10.1242/jeb.023671
[12]
Farrell "Cardiac form, function and physiology" (2017)
[13]
Farrell "Maximum cardiac performance of rainbow trout (Oncorhynchus mykiss) at temperatures approaching their upper lethal limit" J. Exp. Biol. (1996) 10.1242/jeb.199.3.663
[14]
Farrell "Maximum cardiac performance and adrenergic sensitivity of the sea bass Dicentrarchus labrax at high temperatures" J. Exp. Biol. (2007) 10.1242/jeb.002881
[15]
Franklin "Elucidating mechanism is important in forecasting the impact of a changing world on species survival" J. Exp. Biol. (2021) 10.1242/jeb.242284
[16]
Marine heatwaves under global warming

Thomas L. Frölicher, Erich M. Fischer, Nicolas Gruber

Nature 2018 10.1038/s41586-018-0383-9
[17]
Gamperl "Elevated temperature, per se, does not limit the ability of rainbow trout to increase stroke volume" J. Therm. Biol. (2011) 10.1016/j.jtherbio.2010.08.007
[18]
Gerber "Improved mitochondrial function in salmon (Salmo salar) following high temperature acclimation suggests that there are cracks in the proverbial ‘ceiling" Sci. Rep. (2020) 10.1038/s41598-020-78519-4
[19]
Gerber "Acclimation to warm temperatures has important implications for mitochondrial function in Atlantic salmon (Salmo salar)" J. Exp. Biol. (2021) 10.1242/jeb.236257
[20]
Gollock "Cardiovascular and haematological responses of Atlantic cod (Gadus morhua) to acute temperature increase" J. Exp. Biol. (2006) 10.1242/jeb.02319
[21]
Haverinen "Significance of Na+ current in the excitability of atrial and ventricular myocardium of the fish heart" J. Exp. Biol. (2006) 10.1242/jeb.02044
[22]
Haverinen "Reduced ventricular excitability causes atrioventricular block and depression of heart rate in fish at critically high temperatures" J. Exp. Biol. (2020) 10.1242/jeb.225227
[23]
Ho "Assessment of zebrafish cardiac performance using Doppler echocardiography and power angiography" Ultrasound Med. Biol. (2002) 10.1016/s0301-5629(02)00564-1
[24]
Iftikar "Do mitochondria limit hot fish hearts? Understanding the role of mitochondrial function with heat stress in Notolabrus celidotus" PLoS ONE (2013) 10.1371/journal.pone.0064120
[25]
Joaquim "Cardiac function and critical swimming speed of the winter flounder (Pleuronectes americanus) at two temperatures" Comp. Biochem. Physiol. (2004) 10.1016/j.cbpb.2004.03.016
[26]
Johnson "Power output of fish muscle fibres performing oscillatory work: effects of acute and seasonal temperature change" J. Exp. Biol. (1991) 10.1242/jeb.157.1.409
[27]
Johnson "Increasing occurrence of cold and warm extremes during the recent global warming slowdown" Nat. Commun. (2018) 10.1038/s41467-018-04040-y
[28]
The relation between force and speed in muscular contraction

Bernhard Katz

The Journal of Physiology 1939 10.1113/jphysiol.1939.sp003756
[29]
Keen "Blood oxygenation and cardiorespiratory function in steelhead trout (Oncorhynchus mykiss) challenged with an acute temperature increase and zatebradine-induced bradycardia" J. Therm. Biol. (2012) 10.1016/j.jtherbio.2012.01.002
[30]
Keen "Thermal acclimation alters both adrenergic sensitivity and adrenoreceptor density in cardiac tissue of rainbow trout" J. Exp. Biol. (1993) 10.1242/jeb.181.1.27
[31]
Leeuwis "The environmental tolerances and metabolic physiology of sablefish (Anoplopoma fimbria)" Comp. Biochem. Physiol. (Special Aquaculture Issue) (2019) 10.1016/j.cbpa.2019.02.004
[32]
Leeuwis "Research on sablefish (Anoplopoma fimbria) suggests that a limited capacity to increase heart function leaves hypoxic fish susceptible to heat waves" Proc. R. Soc. B (2021) 10.1098/rspb.2020.2340
[33]
Motyka "Long-term hypoxia exposure alters the cardiorespiratory physiology of steelhead trout (Oncorhynchus mykiss), but does not affect their upper thermal tolerance" J. Therm. Biol. (2017) 10.1016/j.jtherbio.2016.03.007
[34]
Penney "Cardiorespiratory responses of seawater-acclimated adult Arctic char (Salvelinus alpinus) and Atlantic salmon (Salmo salar) to an acute temperature increase" Can. J. Fish, Aqua, Sci. (2014) 10.1139/cjfas-2013-0569
[35]
Petersen "Cod (Gadus morhua) cardiorespiratory physiology and hypoxia tolerance following acclimation to low-oxygen conditions" Physiol. Biochem. Zool. (2010) 10.1086/657286
[36]
Roberts "Effects of hypoxic acclimation on contractile properties of the spongy and compact ventricular myocardium of steelhead trout (Oncorhynchus mykiss)" J. Comp. Physiol. B. (2021) 10.1007/s00360-020-01318-w
[37]
Sanchez-Quintana "Morphological analysis of the fish heart ventricle: myocardial and connective tissue architecture in teleost species" Ann. Anat. (1995) 10.1016/s0940-9602(11)80198-6
[38]
Sandblom "Adrenergic control of venous capacitance during moderate hypoxia in the rainbow trout (Oncorhynchus mykiss): role of neural and circulating catecholamines" Am. J. Physiol. Regul. Integr. Comp. Physiol. (2006) 10.1152/ajpregu.00893.2005
[39]
Shiels "The effect of temperature and adrenaline on the relative importance of the sarcoplasmic reticulum in contributing calcium to force development in isolated ventricular trabeculae from rainbow trout" J. Exp. Biol. (1997) 10.1242/jeb.200.11.1607
[40]
Steinhausen "The effect of acute temperature increases on the cardiorespiratory performance of resting and swimming sockeye salmon (Oncorhynchus nerka)" J. Exp. Biol. (2008) 10.1242/jeb.019281
[41]
Syme "Passive viscoelastic work of isolated rat, Rattus norvegicus, diaphragm muscle" J. Physiol. (1990) 10.1113/jphysiol.1990.sp018068
[42]
Syme "Influence of extent of muscle shortening and heart rate on work from frog heart trabeculae" Am. J. Physiol. (1993) 10.1152/ajpregu.1993.265.2.r310
[43]
Syme "Effect of cycle frequency and excursion amplitude on work done by rat diaphragm muscle" Can. J. Physiol. Pharmacol. (1989) 10.1139/y89-206
[44]
Syme "Increased ventricular stiffness and decreased cardiac function in Atlantic cod (Gadus morhua) at high temperatures" Am. J. Physiol. Regul. Integr. Comp. Physiol. (2013) 10.1152/ajpregu.00055.2013
[45]
Szekeres "On the neglected cold side of climate change and what it means to fish" Clim. Res. (2016) 10.3354/cr01404
[46]
Verhille "A heart to heart on temperature: Impaired temperature tolerance of triploid rainbow trout (Oncorhynchus mykiss) due to early onset of cardiac arrhythmia" Comp. Biochem. Physiol. A. Mol. Integr. Physiol. (2013) 10.1016/j.cbpa.2013.01.011
Metrics
10
Citations
46
References
Details
Published
Feb 15, 2022
Vol/Issue
225(4)
License
View
Funding
Natural Sciences and Engineering Research Council of Canada Award: 249926-2011
Memorial University of Newfoundland and Labrador
Cite This Article
A. Kurt Gamperl, Alexander L. Thomas, Douglas A. Syme (2022). Can temperature-dependent changes in myocardial contractility explain why fish only increase heart rate when exposed to acute warming?. Journal of Experimental Biology, 225(4). https://doi.org/10.1242/jeb.243152