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First published online March 14, 2008
Journal of Experimental Biology 211, 1063-1074 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.010181

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The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii

Victoria Matey¹, Jeffrey G. Richards², Yuxiang Wang³, Chris M. Wood⁴, Joe Rogers⁴, Rhiannon Davies³, Brent W. Murray⁵, X.-Q. Chen⁶, Jizeng Du^6,* and Colin J. Brauner^2,

¹ Department of Biology, San Diego State University, San Diego, CA, USA
² Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada
³ Department of Biology, Queen's University, Kingston, Ontario, KZP 3N6, Canada
⁴ Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1, Canada
⁵ Ecosystem Science and Management Program, University of Northern British Columbia, Prince George, BC, V2N 4Z9, Canada
⁶ Department of Biotechnology, Life Science College, Zhejiang University, Hangzhou, Zhejiang 310027, People's Republic of China

^*Author for correspondence in Chinese (e-mail: dujz{at}zju.edu.cn) Author for correspondence (e-mail: brauner{at}zoology.ubc.ca)

Accepted 30 January 2008

Goldfish and crucian carp at low temperature exhibit plasticity in gill morphology during exposure to hypoxia to enhance gas exchange. Hypoxia-induced changes in gill morphology and cellular ultrastructure of the high altitude scaleless carp from Lake Qinghai, China, were investigated to determine whether this is a general characteristic of cold water carp species. Fish were exposed to acute hypoxia (0.3 mg O₂ l^–1) for 24 h followed by 12 h recovery in normoxic water (6 mg O₂ l^–1 at 3200 m altitude), with no mortality. Dramatic alterations in gill structure were initiated within 8 h of hypoxia and almost complete by 24 h, and included a gradual reduction of filament epithelial thickness (>50%), elongation of respiratory lamellae, expansion of lamellar respiratory surface area (>60%) and reduction in epithelial water–blood diffusion distance (<50%). An increase in caspase 3 activity in gills occurred following 24 h exposure to hypoxia, indicating possible involvement of apoptosis in gill remodeling. Extensive gill mucous production during hypoxia may have been part of a general stress response or may have played a role in ion exchange and water balance. The large increase in lamellar surface area and reduction in diffusion distance presumably enhances gas transfer during hypoxia (especially in the presence of increased mucous production) but comes with an ionoregulatory cost, as indicated by a 10 and 15% reduction in plasma [Na⁺] and [Cl^–], respectively, within 12–24 h of hypoxia. Within 12 h of hypoxia exposure, `wavy-convex'-mitochondria rich cells (MRCs) with large apical crypts and numerous branched microvilli were transformed into small `shallow-basin' cells with a flattened surface. As the apical membrane of MRCs is the site for active ion uptake from the water, a reduction in apical crypt surface area may have contributed to the progressive reduction in plasma [Na⁺] and [Cl^–] observed during hypoxia. The changes in the macro- and ultra-structure of fish gills, and plasma [Na⁺] and [Cl^–] during hypoxia were reversible, showing partial recovery by 12 h following return to normoxia. Although the large morphological changes in the gill observed in the scaleless carp support the hypothesis that gill remodeling during hypoxia is a general characteristic of cold water carp species, the reduced magnitude of the response in scaleless carp relative to goldfish and crucian carp may be a reflection of their more active lifestyle or because they reside in a moderately hypoxic environment at altitude.

Key words: gill morphology, hypoxia, ionoregulation, mitochondria rich cell, osmorespiratory compromise

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