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This Article Full Text Full Text (PDF) All Versions of this Article: 297/1/R224    most recent 00189.2009v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Google Scholar Articles by Mitrovic, D. Articles by Perry, S. F. PubMed PubMed Citation Articles by Mitrovic, D. Articles by Perry, S. F.

ARTICLES

Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia

¹Department of Biology, University of Ottawa, Ottawa, Ontario, Canada; ²Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada; and ³Department of Molecular Biosciences, University of Oslo, Oslo, Norway

Submitted 1 April 2009 ; accepted in final form 12 May 2009

Goldfish (Carassius auratus) acclimated to 7°C and exposed to hypoxia (10 mmHg) for 7 days exhibited a pronounced remodeling of the gill consisting of the removal of an interlamellar cell mass (ILCM). Subsequent experiments were designed to assess the impact of gill remodeling and the associated increase in functional lamellar surface area on the distribution of branchial ionocytes and Cl^– flux across the gill. Despite the increased functional lamellar surface area during hypoxia, there was no corresponding increase in Cl^– loss or efflux of the extracellular marker polyethylene glycol (PEG 4000). However, when hypoxic fish were returned to normoxic water for 12 h, rates of Cl^– and PEG efflux were markedly stimulated in keeping with an increased surface area for solute movement. Similarly, the rate of branchial Cl^– uptake was reduced (105 ± 22 vs. 45 ± 8 µmol·kg^–1·h^–1) in normoxic and hypoxic fish, respectively, but then stimulated (345 µmol·kg^–1·h^–1) upon reestablishment of normoxic conditions. Hypoxia (7 days) was accompanied by a significant decrease in the total cross-sectional area of branchial ionocytes owing to a decrease in their numbers and individual sizes. Thus, despite experiencing an increase in functional lamellar surface area, hypoxic goldfish limit branchial Cl^– loss likely by a hypoxia-mediated decrease in paracellular permeability. In normoxic fish, the ionocytes were largely confined to the outer edges of the ILCM. During hypoxia, preexisting ionocytes migrated with the shrinking ILCM, while a smaller proportion of newly differentiated cells appeared below the surface of the ILCM. The capacity to maintain a population of ionocytes in contact with the water is an appropriate strategy to retain ionoregulatory capabilities regardless of whether the lamellae are uncovered or covered.

hypoxia; ion regulation; Cl^– balance; mitochondrion-rich cell; ionocyte; Na⁺/K⁺-ATPase; interlamellar cell mass