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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 Du6,* and Colin J. Brauner2,{dagger}

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


Figure 1
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  		Fig. 1. General view of the scaleless carp gill filaments using scanning electron microscopy (SEM) in fish exposed to normoxia (control; A), following exposure to 0.3 mg O2 l–1 hypoxia for 12 h (B), 24 h (C), and following 12 h recovery in normoxia (D). Note that in A, gill filaments bear short lamellae, in B there is an increase in height and basal length of lamellae, which are accentuated in C, and in D there is a reduction in height and basal length of lamellae relative to C. L, lamella; TE, trailing (afferent) edge of filament. Scale bars, 300 µm.

 

Figure 2
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  		Fig. 2. General view of the scaleless carp gill filaments viewed by light microscopy (LM) in fish exposed to normoxia (control; A), following exposure to 0.3 mg O2 l–1 hypoxia for 12 h (B), 24 h (C), and following 12 h recovery in normoxia (D). Note that in A, the filament is thick and there is an interlamellar mass, in B and C there is a thinning of the filament and lamellar epithelium, and protrusion of the lamellae. In D, there is a thickening of the filament and lamellae, with the reappearance of the interlamellar mass. Scale bars, 20 µm.

 

Figure 3
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  		Fig. 3. Changes in (A) protruding lamellar surface area, (B) water–blood diffusion distance, and (C) filament epithelial thickness in the gills of the scaleless carp during exposure to hypoxia (0.3 mg O2 l–1) for 24 h followed by recovery in normoxia for 12 h. *A statistically significant difference from the normoxic control values. Vertical bars about the mean represent s.e.m. (N=7).

 

Figure 4
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  		Fig. 4. Caspase 3 activity levels in the gills of scaleless carp during exposure to hypoxia (0.3 mg O2 l–1) for 24 h followed by recovery in normoxia for 12 h. *A statistically significant difference from the normoxic control values. Vertical bars above the mean represent s.e.m. (N=7).

 

Figure 5
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  		Fig. 5. Ultrastructure of the filament epithelial cells in normoxic control carp viewed by scanning electron microscopy (SEM; A), and transmission electron microscopy (TEM; B–E). A is the surface of the filament epithelium possessing the `wavy-convex' MRCs with highly ramified microvilli (white arrows) and short and slightly branched microvilli (white-headed arrows), PVCs with complex patterns of microvilli, and a few MCs discharging secretory granules. B is the apical surface of an MRC with highly ramified microvilli, C is the apical surface of an MRC with short microvilli, D is the perinuclear area of an {alpha}- (`light') MRC, and E is the perinuclear area of a β- (`dark') MRC. M, mitochondrion; MC, mucous cell; McV, microvilli; MRC, mitochondria-rich cell; MV, microvesicle; N, nucleus; PVC, pavement cell; RER, rough endoplasmic reticulum; TR, tubular reticulum. Scale bars: (A) 10 µm; (B,C) 1 µm; (D,E) 0.5 µm.

 

Figure 6
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  		Fig. 6. Ultrastructure of filament epithelium viewed by transmission electron microscopy (TEM) in normoxic control carp. (A) Pavement cell with cytoplasm containing microvesicles with a dense core. (B) Mucous cell filled with secretory granules. (C) Immature rodlet cell with developing rodlet granules. GA, Golgi apparatus; M, mitochondrion; MG, mucous granule; MRC, mitochondria-rich cell; PVC, pavement cell; RER, rough endoplasmic reticulum; RG, rodlet granule. Scale bars, 2 µm.

 

Figure 7
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  		Fig. 7. Ultrastructure of the filament epithelium surface viewed by scanning electron microscopy (SEM) in the scaleless carp exposed to hypoxia (0.3 mg O2 l–1) for 4 h (A), 8 h (B), 12 h (C) and 24 h (D). In A and B, note the `wavy-convex' mitochondria-rich cell (MRCs) with short and slightly branched microvilli (arrows) and numerous mucous cells releasing mucous granules; in C, note the small openings of MRCs (arrows), abundant mucous cells, and mucous deposition on the epithelial surface; in D, note `shallow-basin' MRCs (arrows) with a thick film of mucous covering epithelial surface. Scale bars, 10 µm.

 

Figure 8
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  		Fig. 8. Ultrastructure of filament epithelial cells viewed by transmission electron microscopy (TEM) in carp exposed to hypoxia (0.3 mg O2 l–1) for 4 h (A,B) and 8 h (C–F). In A, note the cytoplasm of the {alpha}-mitochondria-rich cell (MRC) containing swollen mitochondria, irregular meshes of tubular reticulum (TR) and high concentrations of ribosomes (R). In B note the apical area of the {alpha}-MRC with short microvilli, formation of microvesicles (arrows), and the concentration of numerous microvesicles under the apical membrane. In C, note neighboring MRC and mucous cell (MC) and abundant microvesicles spreading from apical to perinuclear area of the MRC. In D, note MRC on the bottom of the cavity formed by flanks of the pavement cells (PVCs). In E, note the MRC with small flattened apical surface and high concentration of microvesicles under the apical membrane. In F, note the cytoplasm of the `shallow-basin' {alpha}-MRC. In B,D,E arrows indicates site of microvesicle (MV) formation. RER, rough endoplasmic reticulum; M, mitochondrion. Scale bars, (A) 0.5 µm; (B,D,E) 2 µm; (C,F) 1 µm.

 

Figure 9
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  		Fig. 9. Ultrastructure of mucous (A) and rodlet (B,C) cells in the outermost layer of the filament epithelium viewed by transmission electron microscopy (TEM) in carp exposed to hypoxia (0.3 mg O2 l–1) for 24 h. MC, mucous cell; MV, microvesicle; PVC, pavement cell; RC, rodlet cell; RG, rodlet granule; TR, tubular reticulum. Scale bars, (A,B) 2 µm; (C) 1 µm.

 

Figure 10
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  		Fig. 10. Ultrastructure of the filament epithelium in carp 6 h (A–C) and 12 h (D–F) following recovery from hypoxia as viewed by scanning electron microscopy (SEM; A,D), and transmission electron microscopy (TEM; B,C,E,F). In A, which shows the epithelial surface, note the mucous cells (MCs), `shallow-basin' mitochondria-rich cell (MRCs; black-headed arrows) and `wavy-convex' MRCs with short microvilli (white-headed arrows). In B, note the shallow-basin MRC with branched microvilli protruding from the apical cavity. In C, note the wavy-convex MRC with short, wide, and slightly branched microvilli. In D, which shows the epithelial surface, note the abundant wavy-convex MRCs with branched microvilli (white arrows; McV) and MRCs with short microvilli (white-headed arrows). E and F show the apical area of wavy-convex MRCs with short and strait (E) and branched longer microvilli (F). PVC, pavement cell. Scale bars, (A,D) 10 µm; (B) 2 µm; (C,E,F) 1 µm.

 

Figure 11
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  		Fig. 11. Changes in plasma [Na+] (filled circles) and [Cl–] (open circles) in the scaleless carp during exposure to hypoxia (0.3 mg O2 l–1) for 24 h followed by recovery in normoxia for 12 h. *A statistically significant difference from the normoxic control values; asterisks below the symbols refer to [Cl–], and that above the symbol refers to [Na+]. Vertical bars about the mean represent s.e.m. (N=7).

 

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© The Company of Biologists Ltd 2008