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The pattern of heart rate variability (HRV) within 250 consecutive heartbeat intervals (R-R interval) of a single H. unitaeniatus in (A) normoxia, (B) hypoxia, (C) hypoxia and blockade of adrenergic receptors, and (D) hypoxia and total (adrenergic and cholinergic receptor) blockade. The 250 consecutive R-R intervals are displayed as (i) a tachogram plot, (ii) a frequency histogram in 5·ms bins, and (iii) a power spectrum of the Fourier transform that shows the frequency and power of oscillatory components of the R-R interval tachogram.
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The jeju is a teleost fish with bimodal respiration that utilizes a modified swim bladder as an air-breathing organ (ABO). Like all air-breathing fish studied to date, jeju exhibit pronounced changes in heart rate (fH) during air-breathing events, and it is believed that these may facilitate oxygen uptake (MO2) from the ABO. The current study emplo...
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... This increase in HR is generated by the release of a predominant inhibitory vagal tonus to the heart, resulting from stimulation of stretch receptors associated with the ABO, plus central chemoreceptors 65 (Axelsson et al., 1989;Johansen, 1966;Skals et al., 2006), as is the case for mammals (Jordan & Spyer, 1987;Taylor et al., 1999). Although AB is often discontinuous and arrhythmic in fish (Graham, 1997;Randall et al., 1981), it has been proposed that the associated variations in HR are homologous to RSA in mammals 71 (Graham et al., 1995;McKenzie et al., 2007). After each AB, these fish typically return to the HRV pattern of a water-breathing fish, indicating that the two patterns are separately controlled 69 (Graham, 1997). ...
Mammals show clear changes in heart rate linked to lung ventilation, characterized as respiratory sinus arrhythmia (RSA). These changes are controlled in part by variations in the level of inhibitory control exerted on the heart by the parasympathetic arm of the autonomic nervous system (PNS). This originates from preganglionic neurons in the nucleus ambiguous that supply phasic, respiration-related activity to the cardiac branch of the vagus nerve, via myelinated, efferent fibres with rapid conduction velocities. An elaboration of these central mechanisms, under the control of a 'vagal system' has been endowed by psychologists with multiple functions concerned with 'social engagement' in mammals and, in particular, humans. Long-term study of cardiorespiratory interactions (CRI) in other major groups of vertebrates has established that they all show both tonic and phasic control of heart rate, imposed by the PNS. This derives centrally from neurones located in variously distributed nuclei, supplying the heart via fast-conducting, myelinated, efferent fibres. Water-breathing vertebrates, which include fishes and larval amphibians, typically show direct, 1:1 CRI between heart beats and gill ventilation, controlled from the dorsal vagal motor nucleus. In air-breathing, ectothermic vertebrates, including reptiles, amphibians and lungfish, CRI mirroring RSA have been shown to improve oxygen uptake during phasic ventilation by changes in their respiratory organs' perfusion, due to blood shunt in their undivided hearts. This system may constitute the evolutionary basis of that generating RSA in mammals, which now lacks a major physiological role in respiratory gas exchange, due to their completely divided systemic and pulmonary circulations.
... In average, the heart rate (f H ) pre-AB and post-AB vary from 32 to 50 bpm, respectively (Belão et al. 2011). Expirations related with a bradycardia, followed by tachycardia upon inspirations, had been detected in all air-breathing fish studied (McKenzie et al. 2007). However, the role of such f H variability is not completely understood. ...
This study investigated the dependence of contraction from extracellular Ca2+, the presence of a functional sarcoplasmic reticulum (SR), and the effects of β-adrenergic stimulation using isometric cardiac muscle preparations. Moreover, the expression of Ca2+-handling proteins such as SR-Ca2+-ATPase (SERCA), phospholamban (PLN), and Na+/Ca2+ exchanger (NCX) were also evaluated in the ventricular tissue of adult African sharptooth catfish, Clarias gariepinus, a facultative air-breathing fish. In summary, we observed that (1) contractility was strongly regulated by extracellular Ca2+; (2) inhibition of SR Ca2+-release by application of ryanodine reduced steady-state force production; (3) ventricular myocardium exhibited clear post-rest decay, even in the presence of ryanodine, indicating a decrease in SR Ca2+ content and NCX as the main pathway for Ca2+ extrusion; (4) a positive force-frequency relationship was observed above 60 bpm (1.0 Hz); (5) ventricular tissue was responsive to β-adrenergic stimulation, which caused significant increases in twitch force, kept a linear force-frequency relationship from 12 to 96 bpm (0.2 to Hz), and improved the cardiac pumping capacity (CPC); and (6) African catfish myocardium exhibited similar expression patterns of NCX, SERCA, and PLN, corroborating our findings that both mechanisms for Ca2+ transport across the SR and sarcolemma contribute to Ca2+ activator. In conclusion, this fish species displays great physiological plasticity of E-C coupling, able to improve the ability to maintain cardiac performance under physiological conditions to ecological and/or adverse environmental conditions, such as hypoxic air-breathing activity.
... The exact order in which each fish experienced warming and hypoxia, in the tank or in a respirometer, is provided in Table S1. Fish were observed throughout all exposure protocols, at all exposure levels, through small holes in the curtains (McKenzie et al., 2007b). Care was taken to reduce all disturbance to a minimum during experiments; therefore, experimenters entered at 08:20 h to set up the trials then gave fish 30 min to recover from any disturbance before commencement. ...
... The relatively high f H after surgery presumably indicates an acute stress response, which may have included a release of circulating catecholamines (Reid et al., 1998;Gallo and Civinini, 2003) and/or removal of inhibitory cholinergic neural control (Randall, 1982;reviewed in Farrell, 1984). The progressive decline in f H during the ensuing recovery presumably indicates an associated decline in stress and recovery of autonomic control (Campbell et al., 2004;McKenzie et al., 2007b;Sandblom and Axelsson, 2011;Taylor et al., 2010). Recovery of mean f H by 60 h is somewhat faster than studies on salmonids. ...
Gilthead seabream were equipped with intraperitoneal biologging tags to investigate cardiac responses to hypoxia and warming, comparing when fish were either swimming freely in a tank with conspecifics or confined to individual respirometers. After tag implantation under anaesthesia, heart rate (fH) required 60 hours to recover to a stable value in a holding tank. Subsequently, when undisturbed under control conditions (normoxia, 21°C), mean fH was always significantly lower in the tank than respirometers. In progressive hypoxia (100 - 15% oxygen saturation), mean fH in the tank was significantly lower than respirometers at oxygen levels until 40%, with significant bradycardia in both holding conditions below this. Simultaneous logging of tri-axial body acceleration revealed that spontaneous activity, inferred as the variance of external acceleration (VARm), was low and invariant in hypoxia. Warming (21 to 31°C) caused progressive tachycardia with no differences in fH between holding conditions. Mean VARm was, however, significantly higher in the tank during warming, with a positive relationship between VARm and fH across all temperatures. Therefore, spontaneous activity contributed to raising fH of fish in the tank during warming. Mean fH in respirometers had a highly significant linear relationship with mean rates of oxygen uptake, considering data from hypoxia and warming together. The high fH of confined seabream indicates that respirometry techniques may bias estimates of metabolic traits in some fishes, and that biologging on free-swimming fishes will provide more reliable insight into cardiac and behavioural responses to environmental stressors by fishes in their natural environment.
... Fish were then plugged with two electrocardiogram (ECG) electrodes: the positive one was inserted and sutured in a ventral position between the opercula and the heart, whilst the negative one was placed in a ventrocaudal position, above the pelvic fins (Glass et al. 1991). To allow for pharmacological administrations, a polyethylene cannula (PE50) filled with saline (0.9%) was inserted into the animals' peritoneal cavity through a puncture wound, made with a 21-gauge needle below the negative ECG electrode and sutured to the skin at its exit point (McKenzie et al. 2007;Armelin et al. 2016). Lastly, a second polyethylene cannula (PE100) was inserted into the animals' orobranchial cavity through a role drilled between their nostrils with a Dremel® rotary tool and secured with a cuff (Holeton and Randall 1967;Teixeira et al. 2015). ...
... Myoxocephalus scorpius (Teleostei: Scorpaeniformes) and Hoplerythrinus unitaeniatus (Teleostei: Characiformes) during undisturbed rest (Campbell et al. 2004;McKenzie et al. 2007), in which LF and HF fH oscillations were eliminated by cardiac vagotomy and muscaniric cholinergic blockade, respectively. However, cardiac regulation by sympathetic and NANC efferences cannot be completely disregarded in M. scorpius, because some teleosts have mixed vagal innervation with adrenergic, cholinergic and NANC fibers (Gibbins 1994;Farrell and Smith 2017). ...
Cardiorespiratory adjustments that occur after feeding are essential to supply the demands of digestion in vertebrates. The well-documented postprandial tachycardia is triggered by an increase in adrenergic activity and by non-adrenergic non-cholinergic (NANC) factors in mammals and crocodilians, while it is linked to a withdrawal of vagal drive and NANC factors in non-crocodilian ectotherms – except for fish, in which the sole investigation available indicated no participation of NANC factors. On the other hand, postprandial ventilatory adjustments vary widely among air-breathing vertebrates, with different species exhibiting hyperventilation, hypoventilation, or even no changes at all. Regarding fish, which live in an environment with low oxygen capacitance that requires great ventilatory effort for oxygen uptake, data on the ventilatory consequences of feeding are also scarce. Thus, the present study sought to investigate the postprandial cardiorespiratory adjustments and the mediation of digestion-associated tachycardia in the unimodal water-breathing teleost Oreochromis niloticus. Heart rate (fH), cardiac autonomic tones, ventilation rate (fV), ventilation amplitude, total ventilation and fH/fV variability were assessed both in fasting and digesting animals under untreated condition, as well as after muscarinic cholinergic blockade with atropine and double autonomic blockade with atropine and propranolol. The results revealed that digestion was associated with marked tachycardia in O. niloticus, determined by a reduction in cardiac parasympathetic activity and by circulating NANC factors – the first time such positive chronotropes were detected in digesting fish. Unexpectedly, postprandial ventilatory alterations were not observed, although digestion triggered mechanisms that were presumed to increase oxygen uptake, such as cardiorespiratory synchrony.
... Better comprehension of the nature of HRV, its components, and their relation to the degree of autonomic nervous control on the heart may enable the evaluation of its potential as a tool to improve monitoring of physiological state in a range of vertebrates. HRV has been reported in all vertebrate groups: in elasmobranch and teleost fishes -Scyliorhinus canicula (Taylor and Butler, 1971); short-horned sculpin, Myoxocephalus scorpius (Campbell et (McKenzie et al., 2007); in the lungfish, Lepidosiren paradoxa (Monteiro et al., 2018); in amphibianscururu toad, Rhinella schneideri (Zena et al., 2017); in reptilesrattlesnakes, Crotalus durissus (Campbell et al., 2006;Sanches et al., 2019), lizards -Gallotia galloti (De Vera et al., 2012); in birds -Gallus gallus domesticus (Khandoker et al., 2004), European starling, Sturnus vulgaris (Cyr et al., 2009); and many species of mammals (Giardino et al., 2003; Task Force of The European Society of Cardiology and The North American Society of Pacing and Electrophysiology, 1996;Taylor et al., 2014). ...
Using long-term, remote recordings of heart rate (fH) on fully recovered, undisturbed lizards, we identified several components of heart rate variability (HRV) associated with respiratory sinus arrhythmia (RSA): 1.) A peak in the spectral representation of HRV at the frequency range of ventilation. 2.) These cardiorespiratory interactions were shown to be dependent on the parasympathetic arm of the autonomic nervous system. 3.) Vagal preganglionic neurons are located in discrete groups located in the dorsal motor nucleus of the vagus and also, in a ventro-lateral group, homologous to the nucleus ambiguus of mammals. 4.) Myelinated nerve fibers in the cardiac vagus enabling rapid communication between the central nervous system and the heart. Furthermore, the study of the progressive recovery of fH in tegu following anesthesia and instrumentation revealed that 'resting' levels of mean fH and reestablishment of HRV occurred over different time courses. Accordingly, we suggest that, when an experiment is designed to study a physiological variable reliant on autonomic modulation at its normal, resting level, then postsurgical reestablishment of HRV should be considered as the index of full recovery, rather than mean fH.
... In Jeju, Hoplerythrinus unitaeniatus, the heart rate increased drastically during each air-breath, which was primarily regulated by the withdrawal of an inhibitory cholinergic tone exerted by the parasympathetic innervation via the vagus nerve 68 . However, complete inhibition of cholinergic regulation of heart rate did not affect oxygen uptake in this species 68 . ...
... In Jeju, Hoplerythrinus unitaeniatus, the heart rate increased drastically during each air-breath, which was primarily regulated by the withdrawal of an inhibitory cholinergic tone exerted by the parasympathetic innervation via the vagus nerve 68 . However, complete inhibition of cholinergic regulation of heart rate did not affect oxygen uptake in this species 68 . This regulation merits further investigation as peripheral resistance in the pulmonary artery as well as heart rate is under vagal control in vertebrates having an undivided circulation, including air-breathing fishes, so that lung function would seem highly dependent on cholinergic control 69 . ...
Air‐breathing and amphibious fishes are essential study organisms to shed insight into the required physiological shifts that supported the full transition from aquatic water‐breathing fishes to terrestrial air‐breathing tetrapods. While the origin of air‐breathing in the evolutionary history of the tetrapods has received considerable focus, much less is known about the evolutionary physiology of air‐breathing among fishes. This review summarises recent advances within the field with specific emphasis on the cardiorespiratory regulation associated with air‐breathing and terrestrial excursions, and how respiratory physiology of these living transitional forms are affected by development and personality. Finally, we provide a detailed and re‐evaluated model of the evolution of air‐breathing among fishes that serves as a framework for addressing new questions on the cardiorespiratory changes associated with it. This review highlights the importance of combining detailed studies on piscine air‐breathing model species with comparative multi‐species studies, to add an additional dimension to our understanding of the evolutionary physiology of air‐breathing in vertebrates.
... Conversely, a pronounced rise in heart rate and blood flow during ventilation is well-established in air-breathing tetrapods, particularly in those with episodic breathing (Butler and Jones 1982;Davis 2014;Panneton 2013;Taylor et al. 2014). However, while pronounced cardiorespiratory interactions are well documented in air-breathing fish, irrespective of their air-breathing organ (ABO), there is no information on the cardiac limb of their baroreflex and there is no information on whether blood pressure influences ventilation of the gills or the ABO (Axelsson et al. 1989;Belão et al. 2015;Farrell 1978;Graham et al. 1995;Iversen et al. 2013;McKenzie et al. 2007;Skals et al. 2006;Teixeira et al. 2015). Air-breathing events are associated with a marked increase in ABO perfusion (Axelsson et al. 1989;Bayley et al. 2019;Johansen 1966;Skals et al. 2006;Smith and Gannon 1978). ...
... Nevertheless, the overall relationship between f H and P VA , including the normalized gain, resembles the pattern in amphibians and reptiles ( Fig. 3; Table S1) (Altimiras et al. 1998;Hagensen et al. 2010;Zena et al. 2016a, b), and is consistent with the ubiquitous existence of baroreflexes across jawed vertebrates (Bagshaw 1985;Jones and Milsom 1982;Kent et al. 1972;Reid 1996). P. hypophthalmus displays the archetypical tachycardia during inflation of the swim bladder with minimal changes in blood pressures (Axelsson et al. 1989;Belão et al. 2011Belão et al. , 2015Farrell 1978;Johansen 1966;McKenzie et al. 2007;Singh and Hughes 1973), and we demonstrate that heart rate and ventilatory responses to hypoxia stem from both externally and internally oriented receptors on the gills as common in other teleosts (Florindo et al. 2018;Milsom 2012). Finally, the results reveal that hypotension, induced by SNP infusions, is attended by hyperventilation. ...
... Values are mean ± SEM. Values that do not share a superscript letter differ significantly (p ≤ 0.05) 1 3 cholinergic vagal tone, and in P. hypophthalmus, these responses are abolished by atropine (Fig. 6d) (Axelsson et al. 1989;McKenzie et al. 2007;Taylor et al. 2014). Interestingly, the mean P DA , which increased following atropine injections, decreased to pre-atropine levels post-AB, although blood pressure was maintained in untreated animals (Fig. 6b). ...
All vertebrates possess baroreceptors monitoring arterial blood pressure and eliciting reflexive changes in vascular resistance and heart rate in response to blood pressure perturbations imposed by, e.g., exercise, hypoxia, or hemorrhage. There is considerable variation in the magnitude of the baroreflex amongst vertebrate groups, making phylogenetic trends and association with major evolutionary events such as air-breathing and endothermy, difficult to identify. In the present study, we quantified the baroreflex in the facultative air-breathing catfish Pangasianodon hypophthalmus. Using a pharmacological approach, we quantified the cardiac limb of the baroreflex and by subjecting fish to hypoxia and by stimulation with NaCN with and without pharmacological autonomic blockade; we also examined the cardiovascular regulation associated with air-breathing. As in most other air-breathing fish, air-breathing elicited a substantial tachycardia. This tachycardia was abolished by cholinergic muscarinic pharmacological blockade, which also abolished the cardiac limb of the baroreflex, and consequently such fish failed to maintain their arterial blood pressure when air-breathing. In higher vertebrate classes, baroreceptors elicit ventilatory changes; however, whether this is the case in fish has not previously been investigated. Pangasianodon hypophthalmus demonstrated a prominent increase in ventilation during imposed hypotension. Collectively, these results demonstrate, for the first time, an efficient baroreflex in an air-breathing fish, point towards involvement of baroreceptors in blood pressure regulation during air-breathing, and show a correlation between blood pressure and ventilation, providing additional information on the origin of this link.
... A substantial number of studies on various airbreathing fishes have shown very pronounced cardiorespiratory interactions, where heart rate may double or even triple during the intermittent ventilation of the ABO (101). The tachycardia is associated with a rise in cardiac output (43,71) and hence an elevation of venous return to the heart (101). The rise in heart rate is primarily driven by release of vagal tone, and, in some species, the tachycardia seems to be initiated during expansion of the ABO (29,47). ...
... There are differences in the location, distribution and orientation of these 64 chemoreceptors among species, and their functions may vary depending on the specificity of 65 these cells -such characteristics of fish chemoreceptors and their respective physiological 66 influences have been previously reviewed by Gilmour (2001), Perry and Gilmour (2002), 67 intensity, this progressively depletes venous blood of O 2 (Stevens and Randall 1967;Farrell 136 and Clutterham 2003). In bimodal breathing fishes, this venous hypoxaemia may cause 137 inescapable chemoreflexive stimulation of air-breathing, that increases with intensity as they 138 exercise harder Lefevre et al. 2014 (Hughes and Singh 1970;Johansen et al. 1970;Hughes and 152 Singh 1971;Gee and Graham 1978;Graham and Baird 1982;Smatresk and Cameron 1982;153 Graham and Baird 1984;Pettit and Beitinger 1985;Smatresk 1986;154 Takasusuki, 1994;Brauner et al. 1995;Mattias et al., 1998;Geiger et al. 2000;Kind et al. 2002;155 Seymour et al. 2004;Affonso and Rantin 2005;McKenzie et al., 2007;Lopes et al. 2010;Belão 156 et al. 2011;Lefevre et al. 2011;Belão et al. 2015;Thomsen et al. 2017). It is interesting that, 157 regarding obligate air-breathing fishes, this response varies among actinopterygians (e.g. ...
This review considers the environmental and systemic factors that can stimulate air-breathing responses in fishes with bimodal respiration, and how these may be controlled by peripheral and central chemoreceptors. The systemic factors that stimulate air-breathing in fishes are usually related to conditions that increase the O2 demand of these animals (e.g. physical exercise, digestion and increased temperature), while the environmental factors are usually related to conditions that impair their capacity to meet this demand (e.g. aquatic/aerial hypoxia, aquatic/aerial hypercarbia, reduced aquatic hidrogenionic potential and environmental pollution). It is now well-established that peripheral chemoreceptors, innervated by cranial nerves, drive increased air-breathing in response to environmental hypoxia and/or hypercarbia. These receptors are, in general, sensitive to O2 and/or CO2/H+ levels in the blood and/or the environment. Increased air-breathing in response to elevated O2 demand may also be driven by the peripheral chemoreceptors that monitor O2 levels in the blood. Very little is known about central chemoreception in air-breathing fishes, the data suggest that central chemosensitivity to CO2/H+ is more prominent in sarcopterygians than in actinopterygians. A great deal remains to be understood about control of air-breathing in fishes, in particular to what extent control systems may show commonalities (or not) among species or groups that have evolved air-breathing independently, and how information from the multiple peripheral (and possibly central) chemoreceptors is integrated to control the balance of aerial and aquatic respiration in these animals.
... Though the inhibition of gill ventilation following an air breath is typical of air-breathing teleosts, the lack of a tachycardia is not (Graham 1997). In most other airbreathing fish studied to date, there is a tachycardia immediate following air breaths (Johansen 1966;McKenzie et al. 2007;Lopes et al. 2010;Belão et al. 2011Belão et al. , 2015Taylor et al. 2014), and seems to be associated with a withdrawal of the inhibitory parasympathetic tone on the cardiac pacemaker region (e.g. McKenzie et al. 2007;Iversen et al. 2011;Teixeira et al. 2015). ...
... In most other airbreathing fish studied to date, there is a tachycardia immediate following air breaths (Johansen 1966;McKenzie et al. 2007;Lopes et al. 2010;Belão et al. 2011Belão et al. , 2015Taylor et al. 2014), and seems to be associated with a withdrawal of the inhibitory parasympathetic tone on the cardiac pacemaker region (e.g. McKenzie et al. 2007;Iversen et al. 2011;Teixeira et al. 2015). Stable heart rates following an air breath have been observed in lungfishes and Lepisosteus oculatus (Smatresk and Cameron 1982;Smatresk 1988) as now appears to be the case in C. ornata. ...
The aim of the present study was to determine the roles of externally versus internally oriented CO2/H⁺-sensitive chemoreceptors in promoting cardiorespiratory responses to environmental hypercarbia in the facultative air-breathing fish, Chitala ornata (the clown knifefish). Fish were exposed to environmental acidosis (pH ~ 6.0) or hypercarbia (≈ 30 torr PCO2) that produced changes in water pH equal to the pH levels of the acidotic water to distinguish the relative roles of CO2 versus H⁺. We also injected acetazolamide to elevate arterial levels of PCO2 and [H⁺] in fish in normocarbic water to distinguish between internal and external stimuli. We measured changes in gill ventilation frequency, air breathing frequency, heart rate and arterial blood pressure in response to each treatment as well as the changes produced in arterial PCO2 and pH. Exposure to normocarbic water of pH 6.0 for 1 h did not produce significant changes in any measured variable. Exposure to hypercarbic water dramatically increased air breathing frequency, but had no effect on gill ventilation. Hypercarbia also produced a modest bradycardia and fall in arterial blood pressure. Injection of acetazolamide produced similar effects. Both hypercarbia and acetazolamide led to increases in arterial PCO2 and falls in arterial pH although the changes in arterial PCO2/pH were more modest following acetazolamide injection as were the increases in air breathing frequency. The acetazolamide results suggest that the stimulation of air breathing was due, at least in part, to stimulation of internally oriented CO2/H⁺ chemoreceptors monitoring blood gas changes.
