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First published online May 29, 2009
Journal of Experimental Biology 212, 1949-1964 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.028464

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

Chris M. Wood^1,2,*, Fathima I. Iftikar¹, Graham R. Scott³, Gudrun De Boeck⁴, Katherine A. Sloman⁵, Victoria Matey⁶, Fabiola X. Valdez Domingos⁷, Rafael Mendonça Duarte⁷, Vera M. F. Almeida-Val⁷ and Adalberto L. Val⁷

¹ Department of Biology, McMaster University, Hamilton, Ontario, Canada, L8S 4K1
² Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL 33149, USA
³ Department of Zoology, University of British Columbia, Vancouver, Canada, V6T 1Z4
⁴ Department of Biology, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium
⁵ School of Biological Sciences, University of Plymouth, Devon PL4 8AA, UK
⁶ Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA 92182, USA
⁷ Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil

^* Author for correspondence (e-mail: woodcm{at}mcmaster.ca)

Accepted 16 March 2009

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_O2, indicating a comparable reduction in whole body Na⁺ efflux rate. However, branchial O₂ transfer factor does not fall. The present study focused on the nature of the efflux reduction in the face of maintained gill O₂ permeability. Direct measurements of ²²Na 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_O2=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 [Ca²⁺], became markedly less negative during hypoxia and was restored upon return to normoxia. Ammonia excretion, net K⁺ loss rates, and ³H₂O 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 [³H]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 O₂ exchange capacity during acute hypoxia, a response very different from the traditional osmorespiratory compromise.

Key words: sodium flux, potassium flux, PEG-4000, diffusive water flux, urine flow rate, glomerular filtration rate, gill morphology, mitochondria rich cell, transepithelial potential, fish

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