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

Victoria Matey, Jeffrey G. Richards, Yuxiang Wang, Chris M. Wood, Joe Rogers, Rhiannon Davies, Brent W. Murray, X. Q. Chen, Jizeng Du, Colin J. Brauner

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84 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)1063-1074
Number of pages12
JournalJournal of Experimental Biology
Volume211
Issue number7
DOIs
StatePublished - Apr 2008

Keywords

  • Gill morphology
  • Hypoxia
  • Ionoregulation
  • Mitochondria rich cell
  • Osmorespiratory compromise

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

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    Matey, V., Richards, J. G., Wang, Y., Wood, C. M., Rogers, J., Davies, R., Murray, B. W., Chen, X. Q., Du, J., & Brauner, C. J. (2008). The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. Journal of Experimental Biology, 211(7), 1063-1074. https://doi.org/10.1242/jeb.010181