Autonomic control of post-air-breathing tachycardia in Clarias gariepinus (Teleostei: Clariidae)

Abstract

The African catfish (Clarias gariepinus) is a teleost with bimodal respiration that utilizes a paired suprabranchial chamber located in the gill cavity as an air-breathing organ. Like all air-breathing fishes studied to date, the African catfish exhibits pronounced changes in heart rate (f H) that are associated with air-breathing events. We acquired f H, gill-breathing frequency (f G) and air-breathing frequency (f AB) in situations that require or do not require air breathing (during normoxia and hypoxia), and we assessed the autonomic control of post-air-breathing tachycardia using an infusion of the β-adrenergic antagonist propranolol and the muscarinic cholinergic antagonist atropine. During normoxia, C. gariepinus presented low f AB (1.85 ± 0.73 AB h(-1)) and a constant f G (43.16 ± 1.74 breaths min(-1)). During non-critical hypoxia (PO2 = 60 mmHg), f AB in the African catfish increased to 5.42 ± 1.19 AB h(-1) and f G decreased to 39.12 ± 1.58 breaths min(-1). During critical hypoxia (PO2 = 20 mmHg), f AB increased to 7.4 ± 1.39 AB h(-1) and f G decreased to 34.97 ± 1.78 breaths min(-1). These results were expected for a facultative air breather. Each air breath (AB) was followed by a brief but significant tachycardia, which in the critical hypoxia trials, reached a maximum of 143 % of the pre-AB f H values of untreated animals. Pharmacological blockade allowed the calculation of cardiac autonomic tones, which showed that post-AB tachycardia is predominantly regulated by the parasympathetic subdivision of the autonomic nervous system.

The autonomic control of upright posture tachycardia in the arboreal lizard Iguana iguana

“…For example, the spectrum of Myoxocephalus scorpius (Teleostei; f H of ∼20 bpm) is mainly comprehended between 0.00 and 0.06 Hz (Campbell, Taylor, & Egginton, ), that of Rhinella schneideri (Amphibia; f H of ∼17 bpm) between 0.00 and 0.04 Hz (Zena et al., ), that of I. iguana (Lacertilia; f H of ∼48 bpm) between 0.00 and 0.50 Hz (this study), that of Gallotia galloti (Lacertilia; f H of ∼50 bpm) between 0.00 and 0.50 Hz (De Vera & González, ), that of P. molurus (Serpentes; f H of ∼23 bpm) between 0.00 and 0.15 Hz (Lopes et al., 2017), that of Crocodylus porosus (Crocodylia; f H of ∼17 bpm) between 0.00 and 0.15 Hz (Seebacher & Franklin, ), that of Caiman latirostris (Crocodylia; f H of ∼18 bpm) between 0.00 and 0.15 Hz (Braga et al., ), and that of Ratus norvegicus (Mammalia; f H of ∼300 bpm) between 0.00 and 3.00 Hz (Kuwahara et al., ). This is probably a consequence of interspecific variations in the predominant mode of nervous cardio‐regulation (sympathetic or parasympathetic) (Altimiras, ; Blasco, McKenzie, Taylor, & Rantin, ; Taylor et al., ; Teixeira, Armelin, Abe, Rantin, & Florindo, ), as well as of interspecific differences in basal f H —as animals with reduced f H naturally tend to exhibit less oscillations in this variable in a given period of time (resulting in spectra comprised within a range of lower frequencies).…”

“…molurus (Serpentes; f H of ∼23 bpm) between 0.00 and 0.15 Hz (Lopes et al, 2017), that of Crocodylus porosus (Crocodylia; f H of ∼17 bpm) between 0.00 and 0.15 Hz (Seebacher & Franklin, 2004), that of Caiman latirostris (Crocodylia; f H of ∼18 bpm) between 0.00 and 0.15 Hz (Braga et al, 2016), and that of Ratus norvegicus (Mammalia; f H of ∼300 bpm) between 0.00 and 3.00 Hz (Kuwahara et al, 1994). This is probably a consequence of interspecific variations in the predominant mode of nervous cardio-regulation (sympathetic or parasympathetic) (Altimiras, 1999;Blasco, McKenzie, Taylor, & Rantin, 2017;Taylor et al, 2014;Teixeira, Armelin, Abe, Rantin, & Florindo, 2015), as well as of interspecific differences in basal f H -as animals with reduced f H naturally tend to exhibit less oscillations in this variable in a given period of time (resulting in spectra comprised within a range of lower frequencies). Seymour and Arndt (2004) commented that tilt angles of 30 • and 60 • generate an increase in hydrostatic pressure on the basis of a blood column respectively equivalent to ∼50 and ∼90% of that generated by a 90 • inclination.…”

The influence of midazolam on heart rate arises from cardiac autonomic tones alterations in Burmese pythons, Python molurus

“…Because the HR of ectothermic vertebrates can respond either to classic autonomic neurotransmitters (adrenaline/noradrenaline and acetylcholine) (Leite et al, 2009;Armelin et al, 2014;Taylor et al, 2014;Teixeira et al, 2015) or to non-adrenergic non-cholinergic factors (Wang et al, 2001;Skovgaard et al, 2009;Enok et al, 2012;Braga et al, 2016), it seems difficult to determine the mediators of this case of bradycardia. However, the lack of significant differences among the HR levels of double blocked animals in the four experimental stages performed ( Fig.…”

Control of air-breathing in fishes: Central and peripheral receptors

“…The most commonly observed adjustments to hypoxia/hypoxaemia is a decrease in gill ventilation once air-breathing is initiated (Johansen et al, 1970;Singh, 1976;Randall et al, 1981;Smatresk and Cameron, 1982;Shelton et al, 1986;McKenzie et al, 1991a;Graham, 1997). Also, a hypoxic bradycardia, which is a hallmark in most fishes, gives way to a tachycardia following each air breath, often accompanied by increases in cardiac output and perfusion of the air-breathing organ Singh and Hughes, 1973;Jordan, 1976;Axelsson et al, 1989;Skaals et al, 2006;McKenzie et al, 2007;Nelson et al, 2007;Lopes et al, 2010;Belöo et al, 2011;Iversen et al, 2011;Teixeira et al, 2015).…”