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First published online March 9, 2004
Journal of Experimental Biology 207, 1399-1413 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.00895

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Physiological, biochemical and morphological indicators of osmoregulatory stress in `California' Mozambique tilapia (Oreochromis mossambicus x O. urolepis hornorum) exposed to hypersaline water

Brian A. Sardella^1,*, Victoria Matey², Jill Cooper³, Richard J. Gonzalez³ and Colin J. Brauner¹

¹ Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1Z4 Canada
² Department of Biology, San Diego State University, 5500 Campanile Road, San Diego, CA 92182 USA
³ Department of Biology, University of San Diego, 5998 Alcala Park, San Diego CA, 92110 USA

View larger version (16K): [in a new window]   Fig. 1. The effect of transfer from 25 g l–1 to 35 g l–1 seawater on plasma osmolality, [Na+] and [Cl–] in tilapia hybrids from 0 to 28 days following transfer. *Significant difference relative to 0 h (P<0.001, N=7).

View larger version (185K): [in a new window]   Fig. 2. SEM showing the surface of gill filaments of tilapia adapted to 35–55 g l–1 salinity for 14 days. (A) Middle of gill filament from 35 g l–1-exposed fish; the rectangle marks the area examined on the trailing edge. L, secondary lamellae; LE, leading edge; TE, trailing edge. (B) Filamental epithelial surface from 35 g l–1-exposed fish; arrows indicate the chloride cell apical pits. MC, mucus cells; PC, pavement cell. (C) Filamental epithelial surface in 45 g l–1-exposed fish. (D) Filamental epithelial surface in 55 g l–1-exposed fish. Scale bars: 100 µm (A), 10 µm (B–D).

View larger version (218K): [in a new window]   Fig. 3. TEM showing the chloride cell ultrastructure from the filamental epithelium of tilapia exposed to 35 g l–1 salinity for 14 days. (A) Interlamellar epithelium. AC, accessory cell; CC, mature chloride cell; IC, immature chloride cell; A, apical pit. (B) Multicellular complex formed by mature and accessory chloride cells; arrowhead indicates short apical tight junctions between CC and AC. Arrows indicate long tight junctions between CC and PC. A, apical pit; D, desmosome. (C) Perinuclear cytoplasm of a mature chloride cell. M, mitochondria; TR, tubular reticulum. (D) Apoptotic cell with nuclear and cytoplasm condensation and distention of the tubular reticulum. Scale bars: 1 µm.

View larger version (17K): [in a new window]   Fig. 4. The effect of transfer from 35 g l–1 to 65 g l–1 salinity on plasma osmolality, [Na+] and [Cl–] in tilapia hybrids from 0 to 120 h following transfer. *Significant difference relative to 0 h value (P=0.01, N=7).

View larger version (15K): [in a new window]   Fig. 5. The effect of salinity on plasma osmolality in tilapia hybrids following graded transfers to 45, 35, 55, 65, 75, 85 or 95 g l–1 salinity. Different lines represent sampling times of 3, 24 or 120 h following transfer (see key). *Significant difference relative to 45 g l–1 value (P<0.001, N=7).

View larger version (20K): [in a new window]   Fig. 6. The effect of salinity on (A) Plasma [Cl–] and (B) plasma [Na+] in tilapia hybrids following graded transfers to 45, 35, 55, 65, 75, 85 or 95 g l–1 salinity. Different lines represent sampling times of 3, 24 or 120 h following transfer (see key). *Significant difference relative to 45 g l–1 value (P<0.001, N=7).

View larger version (16K): [in a new window]   Fig. 7. Branchial Na+, K+-ATPase activity measured in tilapia hybrids acclimated to 35, 45, 55, 65 or 85 g l–1 salinity for 120 h. *Significant difference relative to 35 g l–1 value (P<0.001, N=7).

View larger version (181K): [in a new window]   Fig. 8. SEM showing the surface of filamental epithelium in tilapia exposed to (A) 65 g l–1, (B) 75 g l–1, (C) 85 g l–1 and (D) 95 g l–1 salinity for 120 h. Scale bars: 10 µm. PC, pavement cell.

View larger version (105K): [in a new window]   Fig. 9. TEM showing chloride cell ultrastructure in the filament epithelium of tilapia exposed to 45 g l–1 and 55 g l–1 salinity for 120 h. (A) Apical pit (A), formed by interdigitated apex of mature chloride cells (CC) and cytoplasmic projections of accessory cells (AC; asterisks), in fish exposed to 55 g l–1 salinity; arrowheads, short junctions between CCs and ACs. (B) Mature chloride cell with a deeply indented nucleus. Scale bars: 1 µm.

View larger version (216K): [in a new window]   Fig. 10. TEM showing the chloride cell ultrastructure from the filamental epithelium of tilapia exposed to 65 g l–1 salinity for 120 h. (A) Deep apical pit (A) of a multicellular complex formed by interdigitated chloride cells and accessory cells (ACs); arrowheads, short tight junctions; asterisks, projections of ACs. (B) Perinuclear cytoplasm of a mature chloride cell, showing the extensively developed tubular reticulum. (C) Chloride cell at the early stage of apoptosis. (D) Apoptotic chloride cell with a cleft nucleus and highly condensed cytoplasm. Scale bars: 1 µm.

View larger version (184K): [in a new window]   Fig. 11. TEM showing the chloride cell ultrastructure from the filamental epithelium of tilapia exposed to 75 g l–1 salinity for 120 h. (A) Nucleus and perinuclear cytoplasm of an apoptotic chloride cell (CC). (B) Apical pit of multicellular complex that is partially covered by pavement cells (PC) projections; asterisks, cytoplasmic projections of accessory cells (AC). (C) Apical pit (A) that is completely separated from the ambient water by layer of PCs. (D) A multicellular complex without an apical pit; arrowheads indicate desmosomes joining CCs and ACs. (E) Chloride cell degrading by apoptosis. (E) Chloride cell at the final stage of apoptosis. Scale bars: 1 µm.

View larger version (185K): [in a new window]   Fig. 12. TEM showing the chloride cell ultrastructure of the filamental epithelium from tilapia exposed to 85 g l–1 (A,B) and 95 g l–1 (C–G) salinity for 120 h. (A) Perinuclear cytoplasm of a mature chloride cell. (B) Chloride cell at the early stage of degradation by apoptosis. (C) Nucleus and perinuclear cytoplasm of a mature chloride cell. (D) Multicellular complex with a shallow apical pit, formed by a mature cell at the early stage of apoptosis and accessory cell projections. (E) Apoptotic chloride cell. (F) Degenerated chloride cells with condensed cytoplasm, pycnotic nuclei, and distended and ruptured mitochondria. (G) Chloride cells degrading by necrosis. Scale bars: 1 µm.

View larger version (17K): [in a new window]   Fig. 13. Rate of oxygen consumption (O2) measured in tilapia hybrids acclimated for 2 weeks to 35, 55, 75 or 95 g l–1 salinity. Letters indicate significant differences (P<0.001, N=6).

View larger version (16K): [in a new window]   Fig. 14. Drinking rate measured in tilapia hybrids acclimated for 2 weeks to 35, 55, 75 or 95 g l–1 salinity. Letters indicate significant differences (P<0.001, N=6).

View larger version (19K): [in a new window]   Fig. 15. Relative changes in (A) plasma parameters, with values at 65 g l–1 set to 1.0, and (B) cellular parameters, with values at 55 g l–1 set to 1.0.