Circulating catecholamines and cardiorespiratory responses in hypoxic lungfish (Protopterus dolloi): A comparison of aquatic and aerial hypoxia

Abstract

Circulating catecholamine levels and a variety of cardiorespiratory variables were monitored in cannulated bimodally breathing African lungfish (Protopterus dolloi) exposed to aquatic or aerial hypoxia. Owing to the purported absence of external branchial chemoreceptors in lungfish and the minor role played by the gill in O2 uptake, it was hypothesized that plasma catecholamine levels would increase only during exposure of fish to aerial hypoxia. The rapid induction of aquatic hypoxia (final PWO2 = 25.9 ± 1.6 mmHg) did not affect the levels of adrenaline (A) or noradrenaline (NA) within the plasma. Similarly, none of the measured cardiorespiratory variables - including heart rate (fH), blood pressure, air-breathing frequency (fV), O2 consumption (MO2), CO2 excretion (MCO2), or blood gases - were influenced by acute aquatic hypoxia. In contrast, however, the rapid induction of aerial hypoxia (inspired PO2 = 46.6 ± 3.3 mmHg) caused a marked increase in the circulating levels of A (from 7.9 ± 2.0 to 18.8 ± 6.1 nmol L-1) and NA (from 7.7 ± 2.2 to 19.7 ± 6.3 nmol L-1) that was accompanied by significant deceases in MO2, arterial PO2 (PaO2), and arterial O2 concentration (CaO2). Air-breathing frequency was increased (by approximately five breaths per hour) during aerial hypoxia and presumably contributed to the observed doubling of pulmonary MCO2 (from 0.25 ± 0.04 to 0.49 ± 0.07 mmol kg-1 h -1); fH and blood pressure were unaffected by aerial hypoxia. An in situ perfused heart preparation was used to test the possibility that catecholamine secretion from cardiac chromaffin cells was being activated by a direct localized effect of hypoxia. Catecholamine secretion from the chromaffin cells of the heart, while clearly responsive to a depolarizing concentration of KCl (60 mmol L-1), was unaffected by the O 2 status of the perfusion fluid. The results of this study demonstrate that P. dolloi is able to mobilize stored catecholamines and increase fV during exposure to aerial hypoxia while remaining unresponsive to aquatic hypoxia. Thus, unlike in exclusively water-breathing teleosts, P. dolloi would appear to rely solely on internal/airway O2 chemoreceptors for initiating catecholamine secretion and cardiorespiratory responses. © 2005 by The University of Chicago. All rights reserved.