Adenosinergic and cholinergic control mechanisms during hypoxia in the epaulette shark (Hemiscyllium ocellatum), with emphasis on branchial circulation.
Coral reef platforms may become hypoxic at night during low tide. One animal in that habitat, the epaulette shark (Hemiscyllium ocellatum), survives hours of severe hypoxia and at least one hour of anoxia. Here, we examine the branchial effects of severe hypoxia (<0.3 mg oxygen l(-1) for 20 min in anaesthetized epaulette shark), by measuring ventral and dorsal aortic blood pressure (P(VA) and P(DA)), heart rate (fh), and observing gill microcirculation using epi-illumination microscopy. Hypoxia induced a flow of blood in two parallel blood vessels, termed longitudinal vessels, in the outer borders of the free tip of the gill filament. Hypoxia also induced significant falls in fh, P(VA) and P(DA), and a biphasic change in ventilation frequency (increase followed by decrease). Adenosine injection (1 micromol kg(-1)) also initiated blood flow in the longitudinal vessels, in addition to significant drops in P(VA), P(DA) and fh, and a biphasic response in ventilation frequency (decrease followed by increase) indicating that adenosine influences ventilation. Aminophylline (10 mg kg(-1)), an A(1) and A(2) adenosine receptor antagonist, blocked the effects of adenosine injection, and also significantly reduced blood flow in the longitudinal vessels during hypoxia. In the second part of the study, we examined the cholinergic influence on the cardiovascular circulation during severe hypoxia (<0.3 mg l(-1)) using antagonists against muscarinic (atropine 2 mg kg(-1)) and nicotinic (tubocurarine 5 mg kg(-1)) receptors. Injection of acetylcholine (ACh; 1 micromol kg(-1)) into the ventral aorta caused a marked fall in fh, a large increase in P(VA), but small changes in P(DA) (suggesting increased R(gill)). Atropine was able to inhibit the branchial vascular responses to ACh but not the hypoxic bradycardia, suggesting the presence of muscarinic receptors on the heart and gill vasculature, and that the hypoxia induced bradycardia is of non-cholinergic origin. The results suggest that adenosine mediates increases in the arterio-venous circulation in the gill during hypoxia. This may serve to increase blood supply to heart and gill tissue.
Stensløkken
Kåre-Olav
KO
Physiology Programme, Department of Molecular Biosciences, University of Oslo, PO Box 1041, NO-0316 Oslo, Norway. k.o.stenslokken@bio.uio.no
Sundin
Lena
L
Renshaw
Gillian M C
GM
Nilsson
Göran E
GE
D000109:Acetylcholine / Q000494:pharmacology; D000241:Adenosine / Q000037:antagonists & inhibitors / Q000494:pharmacology; D000628:Aminophylline / Q000494:pharmacology; D000704:Analysis of Variance; D000818:Animals; D001285:Atropine / Q000494:pharmacology; D001315:Australia; D001794:Blood Pressure; D005880:Gills / Q000098:blood supply* / Q000502:physiology; D006339:Heart Rate; D000860:Hypoxia / Q000503:physiopathology*; D018727:Muscarinic Antagonists / Q000494:pharmacology; D018733:Nicotinic Antagonists / Q000494:pharmacology; D010140:Pacific Ocean; D012039:Regional Blood Flow / Q000187:drug effects; D012754:Sharks / Q000502:physiology*; D014403:Tubocurarine / Q000494:pharmacology; D014741:Video Recording
D018727:Muscarinic Antagonists; D018733:Nicotinic Antagonists; D000628:Aminophylline; D001285:Atropine; D000241:Adenosine; D000109:Acetylcholine; D014403:Tubocurarine