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First published online November 19, 2007
Journal of Experimental Biology 210, 4224-4232 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.009266

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The autonomic control and functional significance of the changes in heart rate associated with air breathing in the jeju, Hoplerythrinus unitaeniatus

D. J. McKenzie^1,*, H. A. Campbell², E. W. Taylor³, M. Micheli⁴, F. T. Rantin⁴ and A. S. Abe⁵

¹ Institut des Sciences de l'Evolution de Montpellier, UMR 5554 CNRS-Université Montpellier II, Station Méditerranéenne de l'Environnement Littoral, 1 quai de la Daurade, 34200 Sète, France
² School of Integrative Biology, University of Queensland, Brisbane, QL 4072, Australia
³ School of Biosciences, University of Birmingham, Birmingham, B15 2TT, UK
⁴ Department of Physiological Sciences, Federal University of São Carlos, São Carlos, Brazil
⁵ Departamento de Zoologia, Centro de Aquicultura, UNESP, Rio Claro, São Paulo, Brazil

^* Author for correspondence (e-mail: david.mckenzie{at}univ-montp2.fr)

Accepted 19 September 2007

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 (f_H) during air-breathing events, and it is believed that these may facilitate oxygen uptake (M_O2) from the ABO. The current study employed power spectral analysis (PSA) of f_H patterns, coupled with instantaneous respirometry, to investigate the autonomic control of these phenomena and their functional significance for the efficacy of air breathing. The jeju obtained less than 5% of total M_O2 (M_tO2) from air breathing in normoxia at 26°C, and PSA of beat-to-beat variability in f_H revealed a pattern similar to that of unimodal water-breathing fish. In deep aquatic hypoxia (water P_O2=1 kPa) the jeju increased the frequency of air breathing (f_AB) tenfold and maintained M_tO2 unchanged from normoxia. This was associated with a significant increase in heart rate variability (HRV), each air breath (AB) being preceded by a brief bradycardia and then followed by a brief tachycardia. These f_H changes are qualitatively similar to those associated with breathing in unimodal air-breathing vertebrates. Within 20 heartbeats after the AB, however, a beat-to-beat variability in f_H typical of water-breathing fish was re-established. Pharmacological blockade revealed that both adrenergic and cholinergic tone increased simultaneously prior to each AB, and then decreased after it. However, modulation of inhibitory cholinergic tone was responsible for the major proportion of HRV, including the precise beat-to-beat modulation of f_H around each AB. Pharmacological blockade of all variations in f_H associated with air breathing in deep hypoxia did not, however, have a significant effect upon f_AB or the regulation of M_tO2. Thus, the functional significance of the profound HRV during air breathing remains a mystery.

Key words: air breathing, heart rate variability, teleost