Long-term hypoxia exposure alters the cardiorespiratory physiology of steelhead trout ( Oncorhynchus mykiss ), but does not affect their upper thermal tolerance

Motyka, Roman; Norin, Tommy; Petersen, Lene H.; Huggett, Duane B.; Gamperl, A. Kurt

doi:10.1016/j.jtherbio.2016.03.007

Cited by 65 publications

(54 citation statements)

References 69 publications

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“…For commonly studied temperatures, our findings regarding f H , ṀO 2 and autonomic tone align well with current literature. For example, the increase in routine f H and ṀO 2 that we observed with acute warming is well documented for salmonids, typically increasing with Q 10 coefficients of between 1.5 and 2.5 for f H and 2 and 4 for ṀO 2 , as found here (Eliason and Anttila, 2017;Motyka et al, 2017;Penney et al, 2014;Rodnick et al, 2004;Steinhausen et al, 2008). While substantial variation in absolute ṀO 2 and f H values can exist among studies given variable genetic (e.g.…”

Section: Discussionsupporting

confidence: 77%

“…Almost universally among these strategies is an increase in heart rate ( f H ), a response that has been found in Arctic, Antarctic, tropical and temperate species (Eliason and Anttila, 2017;Farrell and Smith, 2017). Furthermore, where measured, the increase in f H mediates an increase in cardiac output ð _ QÞ (Brett, 1971;Ekström et al, 2016;Motyka et al, 2017;Penney et al, 2014;Steinhausen et al, 2008), which presumably services the increased tissue oxygen consumption, as inferred from a proportional increase in wholeanimal oxygen uptake (Ekström et al, 2014;Eliason and Anttila, 2017;Farrell, 2009;Farrell and Smith, 2017;Sandblom et al, 2016a). However, as fish approach their upper thermal limit, f H reaches a peak and thereafter may decline and become arrhythmic (Anttila et al, 2014;Badr et al, 2016;Casselman et al, 2012;Ekström et al, 2014;Eliason et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 77%

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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“…Hypoxic acclimation in Atlantic salmon did not result in significant changes in resting Ṁ O 2 (figure 1a), as shown previously in rainbow trout [24,36], nor in arterial O 2 transport (electronic supplementary material, figure S5) compared with royalsocietypublishing.org/journal/rspb Proc. R. Soc.…”

Section: Discussionsupporting

confidence: 83%

“…If teleosts use b-NHE short-circuiting to increase Ṁ O 2 /Q during exercise, we would predict that the inhibition of paCA in vivo will either result in a decrease in Ṁ O 2 or in a compensatory increase in Q to maintain Ṁ O 2 and swimming speed. In addition, previous studies on several teleost species have shown that Ṁ O 2 /Q increased following hypoxic acclimation, as these fish were unable to increase Q to the same extent as normoxia-acclimated conspecifics [23], yet attained the same aerobic performance in terms of maximal Ṁ O 2 , critical swimming speed (U crit ) and critical thermal maximum (CT max ) [24][25][26]. If the increase in Ṁ O 2 /Q after hypoxic acclimation is also achieved by b-NHE short-circuiting, we would predict a greater reliance of these animals on paCA to support tissue O 2 extraction, compared with normoxia-acclimated fish.…”

Section: Introductionmentioning

confidence: 90%

“…Anaesthetized fish were instrumented with a dorsal aortic catheter [27] and a Doppler flow probe was fitted around the ventral aorta [24] (see electronic supplementary material for details). After surgery, fish were housed individually and allowed to recover for 48 h. In the evening before the swim trials, fish were lightly anaesthetized and transferred to a 81 l Blazka-type swim tunnel, described by Petersen & Gamperl [25].…”

Section: (B) Surgery and Recoverymentioning

confidence: 99%

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Functional support for a novel mechanism that enhances tissue oxygen extraction in a teleost fish

et al. 2019

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A successful spawning migration in salmon depends on their athletic ability, and thus on efficient cardiovascular oxygen (O 2 ) transport. Most teleost fishes have highly pH-sensitive haemoglobins (Hb) that can release large amounts of O 2 when the blood is acidified at the tissues. We hypothesized that plasma-accessible carbonic anhydrase ( paCA; the enzyme that catalyses proton production from CO 2 ) is required to acidify the blood at the tissues and promote tissue O 2 extraction. Previous studies have reported an elevated tissue O 2 extraction in hypoxia-acclimated teleosts that may also be facilitated by paCA. Thus, to create experimental contrasts in tissue O 2 extraction, Atlantic salmon were acclimated to normoxia or hypoxia (40% air saturation for more than six weeks), and the role of paCA in enhancing tissue O 2 extraction was tested by inhibiting paCA at rest and during submaximal exercise. Our results show that: (i) in both acclimation groups, the inhibition of paCA increased cardiac output by one-third, indicating a role of paCA in promoting tissue O 2 extraction during exercise, recovery and at rest; (ii) the recruitment of paCA was plastic and increased following hypoxic acclimation; and (iii) maximal exercise performance in salmon, and thus a successful spawning migration, may not be possible without paCA.

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Effects of acute hypoxia exposure and acclimation on the thermal tolerance of an imperiled Canadian minnow

Reemeyer,

Chapman

2024

J Exp Zool Pt A

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Elevated water temperatures and low dissolved oxygen (hypoxia) are pervasive stressors in aquatic systems that can be exacerbated by climate change and anthropogenic activities, and there is growing interest in their interactive effects. To explore this interaction, we quantified the effects of acute and long‐term hypoxia exposure on the critical thermal maximum (CTmax) of Redside Dace (Clinostomus elongatus), a small‐bodied freshwater minnow with sparse populations in the Great Lakes Basin of Canada and designated as Endangered under Canada's Species at Risk Act. Fish were held at 18°C and acclimated to four levels of dissolved oxygen (>90%, 60%, 40%, and 20% air saturation). CTmax was measured after 2 and 10 weeks of acclimation and after 3.5 weeks of reoxygenation, and agitation behavior was quantified during CTmax trials. Aquatic surface respiration behavior was also quantified at 14 weeks of acclimation to oxygen treatments. Acute hypoxia exposure decreased CTmax in fish acclimated to normoxia (>90% air saturation), but acclimation to hypoxia reduced this effect. There was no effect of acclimation oxygen level on CTmax when measured in normoxia, and there was no effect of exposure time to hypoxia on CTmax. Residual effects of hypoxia acclimation on CTmax were not seen after reoxygenation. Agitation behavior varied greatly among individuals and was not affected by oxygen conditions. Fish performed aquatic surface respiration with low frequency, but performed it earlier when acclimated to higher levels of oxygen. Overall, this work sheds light on the vulnerability of fish experiencing acute hypoxia and heat waves concurrently.

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Long-term hypoxia exposure alters the cardiorespiratory physiology of steelhead trout ( Oncorhynchus mykiss ), but does not affect their upper thermal tolerance

Cited by 65 publications

References 69 publications

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

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

Functional support for a novel mechanism that enhances tissue oxygen extraction in a teleost fish

Effects of acute hypoxia exposure and acclimation on the thermal tolerance of an imperiled Canadian minnow

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