Regulation of gill transcellular permeability and renal function during acute hypoxia in the Amazonian oscar (Astronotus ocellatus): new angles to the osmorespiratory compromise

Abstract

Earlier studies demonstrated that oscars, endemic to ion-poor Amazonian waters, are extremely hypoxia tolerant, and exhibit a marked reduction in active unidirectional Na(+) uptake rate (measured directly) but unchanged net Na(+) balance during acute exposure to low P(O(2)), indicating a comparable reduction in whole body Na(+) efflux rate. However, branchial O(2) transfer factor does not fall. The present study focused on the nature of the efflux reduction in the face of maintained gill O(2) permeability. Direct measurements of (22)Na appearance in the water from bladder-catheterized fish confirmed a rapid 55% fall in unidirectional Na(+) efflux rate across the gills upon acute exposure to hypoxia (P(O(2))=10-20 torr; 1 torr=133.3 Pa), which was quickly reversed upon return to normoxia. An exchange diffusion mechanism for Na(+) is not present, so the reduction in efflux was not directly linked to the reduction in Na(+) influx. A quickly developing bradycardia occurred during hypoxia. Transepithelial potential, which was sensitive to water [Ca(2+)], became markedly less negative during hypoxia and was restored upon return to normoxia. Ammonia excretion, net K(+) loss rates, and (3)H(2)O exchange rates (diffusive water efflux rates) across the gills fell by 55-75% during hypoxia, with recovery during normoxia. Osmotic permeability to water also declined, but the fall (30%) was less than that in diffusive water permeability (70%). In total, these observations indicate a reduction in gill transcellular permeability during hypoxia, a conclusion supported by unchanged branchial efflux rates of the paracellular marker [(3)H]PEG-4000 during hypoxia and normoxic recovery. At the kidney, glomerular filtration rate, urine flow rate, and tubular Na(+) reabsorption rate fell in parallel by 70% during hypoxia, facilitating additional reductions in costs and in urinary Na(+), K(+) and ammonia excretion rates. Scanning electron microscopy of the gill epithelium revealed no remodelling at a macro-level, but pronounced changes in surface morphology. Under normoxia, mitochondria-rich cells were exposed only through small apical crypts, and these decreased in number by 47% and in individual area by 65% during 3 h hypoxia. We suggest that a rapid closure of transcellular channels, perhaps effected by pavement cell coverage of the crypts, allows conservation of ions and reduction of ionoregulatory costs without compromise of O(2) exchange capacity during acute hypoxia, a response very different from the traditional osmorespiratory compromise.