Regulation of the cardiorespiratory system of common carp (Cyprinus carpio) during severe hypoxia at three seasonal acclimation temperatures.
Little is known of the cardiorespiratory control mechanisms utilized by hypoxia-tolerant teleost fish to tolerate prolonged periods (h) of near anoxic exposure. Here, we report on the cardiorespiratory control mechanisms of the common carp Cyprinus carpio L. during normoxia and prolonged, severe hypoxic (<0.3 mg O(2) L(-1)) exposure at acclimation temperatures of 5 degrees C, 10 degrees C, and 15 degrees C. Through serial intra-arterial injections of alpha - and beta -adrenergic, cholinergic, and purinergic antagonists while measuring cardiac output (Q), heart rate (f(H)), ventral aortic blood pressure, and respiration rate, we established that autonomic cardiovascular and respiratory control was preserved during severe hypoxia at all three acclimation temperatures and contributed to downregulation of cardiorespiratory activity. Specifically, inhibitory cholinergic tone mediated up to 76% reductions in f(H) and Q during hypoxia, whereas the accompanying arterial hypotension was attenuated by an upregulation of an alpha -adrenergically mediated peripheral vasoconstriction. Despite the overall cardiac downregulation, a large, stimulatory cardiac beta -adrenergic tone was present during prolonged, severe hypoxia, possibly to protect the heart from attendant acidotic conditions. Purinergic blockade, following alpha -adrenergic and cholinergic antagonists, showed that the hypoxic ventilatory depression, which reversed the 2.3- to 7.7-fold increases in respiration rate that occurred with the onset of hypoxia, was a result of purinergic inhibition at all three acclimation temperatures. In contrast, purinergic inhibition of cardiac activity during hypoxia might be important only at 5 degrees C. Finally, given that cardiac power output was reduced 72%-87% during prolonged, severe hypoxia and that glycolysis yields approximately 94% less ATP per mole glucose than oxidative phosphorylation, it seems unlikely that the common carp sufficiently reduces its cardiac energy demand to a level to preclude activation of a partial Pasteur effect. This means that glycogen stores will be used and waste products will accumulate at faster rates, a finding that may help explain why the common carp cannot tolerate such extended periods of severe hypoxia (weeks to months) at cold acclimation temperatures as the freshwater turtle, which is able to reduce its cardiac energy demand to a level that does not require a Pasteur effect and also blunts autonomic cardiovascular control.
Stecyk
J A W
JA
Department of Zoology, University of British Columbia, Vancouver, Canada. jstecyk@interchange.ubc.ca
Farrell
A P
AP
D000064:Acclimatization / Q000502:physiology*; D000317:Adrenergic alpha-Antagonists / Q000494:pharmacology; D000319:Adrenergic beta-Antagonists / Q000494:pharmacology; D000628:Aminophylline / Q000494:pharmacology; D000818:Animals; D001285:Atropine / Q000494:pharmacology; D001794:Blood Pressure / Q000502:physiology; D002302:Cardiac Output / Q000502:physiology; D002316:Cardiotonic Agents / Q000494:pharmacology; D002320:Cardiovascular Physiological Phenomena; D002347:Carps / Q000502:physiology*; D006339:Heart Rate / Q000502:physiology; D000860:Hypoxia / Q000503:physiopathology; D010646:Phentolamine / Q000494:pharmacology; D011433:Propranolol / Q000494:pharmacology; D012119:Respiration; D013696:Temperature
D000317:Adrenergic alpha-Antagonists; D000319:Adrenergic beta-Antagonists; D002316:Cardiotonic Agents; D000628:Aminophylline; D001285:Atropine; D011433:Propranolol; D010646:Phentolamine