Gill morphology and acute hypoxia: responses of mitochondria-rich, pavement, and mucous cells in the Amazonian oscar (Astronotus ocellatus) and the rainbow trout (Oncorhynchus mykiss), two species with very different approaches to the osmo-respiratory compromise

Author:

Matey Victoria1,Iftikar Fathima I.2,De Boeck Gudrun3,Scott Graham R.4,Sloman Katherine A.5,Almeida-Val Vera M.F.6,Val Adalberto L.6,Wood Chris M.27

Affiliation:

1. Department of Biology, Center for Inland Waters, San Diego State University, San Diego, CA 92182-4614, USA.

2. Department of Biology, McMaster University, Hamilton, ON L8S 4K1, Canada.

3. Department of Biology, University of Antwerp, Groenenborgerlaan 171, B-2020 Antwerp, Belgium.

4. Department of Zoology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.

5. School of Sciences, University of West of Scotland, Paisley, Scotland, PA1 2BE, UK.

6. Laboratory of Ecophysiology and Molecular Evolution, Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil.

7. Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, FL 33149, USA.

Abstract

The hypoxia-intolerant rainbow trout ( Oncorhynchus mykiss (Walbaum, 1792)) exhibits increased branchial ion permeability and Na+influx during acute exposure to moderate hypoxia (Po2 = 80 torr; 1 torr = 133.3224 Pa), manifesting the usual trade-off between gas exchange and electrolyte conservation. In contrast, the hypoxia-tolerant oscar ( Astronotus ocellatus (Agassiz, 1831)) is unusual in exhibiting decreased branchial ion permeability to ions and Na+influx during acute exposure to severe hypoxia (Po2 = 10–20 torr). These different physiological approaches to the osmo-respiratory compromise correlate with rapid, oppositely directed changes in gill morphology. In oscar, pavement cells (PVCs) expanded, partially covering neighboring mitochondria-rich cells (MRCs), which were recessed and reduced in size. Those remaining open were transformed from “shallow-basin” to “deep-hole” forms with smaller openings, deeper apical crypts, and smaller numbers of subapical microvesicles, changes that were largely reversed during normoxic recovery. In contrast, moderate hypoxia caused outward bulging of MRCs in rainbow trout with increases in size, surface exposure, and number of subapical microvesicles, accompanied by PVC retraction. These changes were partially reversed during normoxic recovery. In both rainbow trout and oscar, hypoxia caused discharge of mucus from enlarged mucous cells (MCs). Rapid, divergent morphological changes play an important role in explaining two very different physiological approaches to the osmo-respiratory compromise.

Publisher

Canadian Science Publishing

Subject

Animal Science and Zoology,Ecology, Evolution, Behavior and Systematics

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