Effects of extracellular changes on spontaneous heart rate of normoxia-and anoxia-acclimated turtles (<i>Trachemys scripta</i>)

Stecyk, Jonathan A. W.; Farrell, Anthony P.

doi:10.1242/jeb.02653

Cited by 25 publications

(30 citation statements)

References 54 publications

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“…However, there are tissue-specific differences in the use of metabolic rate suppression among species. For example, in the heart of turtles, anoxia exposure induces metabolic rate suppression resulting in a reduction of cardiac performance to roughly 5% of its normal level (Stecyk and Farrell, 2007), whereas in the anoxic crucian carp , heart performance remained close to routine levels because of a large capacity for anaerobic ATP generation. Despite these tissue-specific differences, whole animal metabolic rate is still suppressed in both the crucian carp and turtle.…”

Section: The Metabolic Challenge Of Surviving O 2 Tensions Below P Critmentioning

confidence: 99%

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Richards

2011

Journal of Experimental Biology

262

202

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SummaryHypoxia survival in fish requires a well-coordinated response to either secure more O 2 from the hypoxic environment or to limit the metabolic consequences of an O 2 restriction at the mitochondria. Although there is a considerable amount of information available on the physiological, behavioral, biochemical and molecular responses of fish to hypoxia, very little research has attempted to determine the adaptive value of these responses. This article will review current attempts to use the phylogenetically corrected comparative method to define physiological and behavioral adaptations to hypoxia in intertidal fish and further identify putatively adaptive biochemical traits that should be investigated in the future. In a group of marine fishes known as sculpins, from the family Cottidae, variation in hypoxia tolerance, measured as a critical O 2 tension (P crit ), is primarily explained by variation in mass-specific gill surface area, red blood cell hemoglobin-O 2 binding affinity, and to a lesser extent variation in routine O 2 consumption rate (M O2 ). The most hypoxia-tolerant sculpins consistently show aquatic surface respiration (ASR) and aerial emergence behavior during hypoxia exposure, but no phylogenetically independent relationship has been found between the thresholds for initiating these behaviors and P crit . At O 2 levels below P crit , hypoxia survival requires a rapid reorganization of cellular metabolism to suppress ATP consumption to match the limited capacity for O 2 -independent ATP production. Thus, it is reasonable to speculate that the degree of metabolic rate suppression and the quantity of stored fermentable fuel is strongly selected for in hypoxia-tolerant fishes; however, these assertions have not been tested in a phylogenetic comparative model.

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Section: The Metabolic Challenge Of Surviving O 2 Tensions Below P Critmentioning

confidence: 99%

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Richards

2011

Journal of Experimental Biology

262

202

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“…Similarly, adenosinergic cardiac inhibition is not involved either (59). Instead, the suggestion has been made that intrinsic electrophysiological changes account for the anoxic depression of cardiac activity in cold-acclimated turtles (20,41,56). Certainly, an increased prevalence of atrial-ventricular blocks, a phenomenon in which ventricular contraction rate is less than the atrial contraction rate, in isolated turtle hearts during anoxia exposure (25) suggests a reduced ventricular excitability and/or a delay or blockage of electrical impulses through the atrial-ventricular node.…”

mentioning

confidence: 99%

“…To mimic in vivo blood plasma pH of anoxiaexposed turtles, cardiac APs were rerecorded for anoxia-acclimated hearts after a switch to a combined acidotic and anoxic saline. This was done to investigate the effect of acidosis on turtle cardiac APs given the reported temperature dependency of its negative inotropic and chronotropic effects on the turtle myocardium (41,49,56,71,73). For sarcolemmal ion channel current recordings, we focused on ventricular myocytes because the ventricle is the power-generating tissue of the turtle heart.…”

mentioning

confidence: 99%

Effect of temperature and prolonged anoxia exposure on electrophysiological properties of the turtle (Trachemys scripta) heart

Stecyk¹,

Paajanen²,

Farrell³

et al. 2007

American Journal of Physiology-Regulatory, Integrative and Comp

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Cardiac activity of the turtle (Trachemys scripta) is greatly depressed with cold acclimation and anoxia. We examined what electrophysiological modifications accompany and perhaps facilitate this depression of cardiac activity. Turtles were first acclimated to 21 degrees C or 5 degrees C and held under either normoxic or anoxic (6 h at 21 degrees C; 14 days at 5 degrees C) conditions. We then measured cardiac action potentials (APs) using spontaneously contracting whole heart preparations and whole cell current densities of sarcolemmal ion channels using isolated ventricular myocytes under appropriate normoxic and anoxic conditions. Compared with 21 degrees C-acclimated turtles, 5 degrees C-acclimated turtles exhibited a less negative resting membrane potential (by 18-29 mV), a 4.7- to 6.8-fold slower AP upstroke rate, and a 4.2- to 4.9-fold greater AP duration. Correspondingly, peak densities of ventricular voltage-gated Na(+) (I(Na)) and L-type Ca(2+) currents and inward slope conductances of inward rectifier K(+) (I(K1)) channel current were approximately 1/7th (Q(10) = 3.4), 1/13th (Q(10) = 5.0), and one-half (Q(10) = 1.4) of those of 21 degrees C-acclimated ventricular myocytes, respectively. With anoxia at 21 degrees C, peak I(Na) density doubled and ventricular AP duration increased by 47%, a change proportional to the reported approximately 30% reduction of intrinsic heart rate. In contrast, with anoxia at 5 degrees C, ventricular AP characteristics were unaffected; of the ion currents investigated, only the inward conductance via I(K1) changed significantly (reduced by 46%). The present findings indicate that cold temperature, more so than prolonged anoxia, results in substantial modifications of cardiac APs and reduction of ventricular ion current densities. These changes likely prepare cardiac muscle for winter anoxia conditions.

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“…Similarly, the European eel (Anguilla anguilla) can maintain cardiac output during a graded hypercapnic acidosis down to an arterial pH of 7.2 (18), and maximal in situ cardiac performance of the armoured catfish (Pterygoplichths pardalis) is not compromised by hypercapnic acidosis until extracellular pH is decreased to 7.1 (11). For the freshwater turtles, cold acclimation preconditions the heart for anoxia and acidosis (26,37), and hearts from anoxia-tolerant species are more tolerant to, and recover better from, combined anoxia and acidosis than those from hypoxia-sensitive species (9).…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, the possible, but to the best of our knowledge previously unexamined, changes in crucian carp blood composition with prolonged anoxia exposure (i.e., hyperkalemia, hypercalcemia, increased adrenaline concentration) were not examined in concert with the anoxic and acidotic stressors. Such potential changes in blood composition could theoretically augment or diminish the effects of anoxia and acidosis on the intrinsic contractile properties of the carp heart reported here [e.g., (1,26,37)]. …”

Section: Methodsmentioning

confidence: 99%

Intrinsic contractile properties of the crucian carp (Carassius carassius) heart during anoxic and acidotic stress

Stecyk

Larsen

Nilsson

2011

American Journal of Physiology-Regulatory, Integrative and Comp

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The crucian carp (Carassius carassius) seems unique among vertebrates in its ability to maintain cardiac performance during prolonged anoxia. We investigated whether this phenomenon arises in part from a myocardium tolerant to severe acidosis or because the anoxic crucian carp heart may not experience a severe extracellular acidosis due to the fish's ability to convert lactate to ethanol. Spontaneously contracting heart preparations from cold-acclimated (6-8°C) carp were exposed (at 6.5°C) to graded or ungraded levels of acidosis under normoxic or anoxic conditions and intrinsic contractile performance was assessed. Our results clearly show that the carp heart is tolerant of acidosis as long as oxygen is available. However, heart rate and contraction kinetics of anoxic hearts were severely impaired when extracellular pH was decreased below 7.4. Nevertheless, the crucian carp heart was capable of recovering intrinsic contractile performance upon reoxygenation regardless of the severity of the anoxic + acidotic insult. Finally, we show that increased adrenergic stimulation can ameliorate, to a degree, the negative effects of severe acidosis on the intrinsic contractile properties of the anoxic crucian carp heart. Combined, these findings indicate an avoidance of severe extracellular acidosis and adrenergic stimulation are two important factors protecting the intrinsic contractile properties of the crucian carp heart during prolonged anoxia, and thus likely facilitate the ability of the anoxic crucian carp to maintain cardiac pumping.

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Effects of extracellular changes on spontaneous heart rate of normoxia-and anoxia-acclimated turtles (Trachemys scripta)

Cited by 25 publications

References 54 publications

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia

Effect of temperature and prolonged anoxia exposure on electrophysiological properties of the turtle (Trachemys scripta) heart

Intrinsic contractile properties of the crucian carp (Carassius carassius) heart during anoxic and acidotic stress

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