Abstract
The toxic effects of Cd2+ on Ca2+ influx kinetics in developing tilapia (Oreochromis mossambicus) larvae were evaluated. Addition of 20 µg l-1 of Cd2+ to the environment of 0 and 3 day-old larvae competitively inhibited the Ca2+ uptake within 4h resulting in a great increase in Km values for Ca2+ influx (19.3 and 17.4 fold, respectively) as compared with their respective controls. Consequently, the actual Ca2+ influx of larvae in solutions of 0.2 mM Ca2+ are suppressed by 32–45%. Also, 3 day-old larvae were more sensitive to internally accumulated Cd2+ than 0 day-old larvae. Although the Ca2+ influx in 0 and 3 day-old larvae may be restored to the levels of their respective controls with 24h of being transferred to a 20 µg l-1 Cd2+ solution, total body Ca2+ content was significantly reduced in 3 day-old larvae. Increased Ca2+ uptake efficiency ensures sufficient Ca2+ for normal growth. However, rapid increase in Ca2+ influx after hatching also leads to higher Cd2+ uptake. Exposure to Cd2+ will lead to a drop in body Ca2+ content resulting in retardation of larval growth. Therefore, we conclude that if Ca2+ uptake is interfered with at this critical stage of development, larvae will not be able to maintain normal levels of body Ca2+ and will show signs of Cd2+ poisoning.
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Atchison, G.J., Henry, M.G. and Sandheinrich, M.B. 1987. Effects of metals on fish behavior: a review. Environ. Biol. Fish. 18: 11–25.
Avella, M., Masoni, A., Bornancin, M. and Mayer-Gostan, N. 1987. Gill morphology and sodium influx in the rainbow trout (Salmo gairdneri) acclimated to artificial freshwater environments. J. Exp. Zool. 241: 159–169.
Ayson, F.G., Kaneko, T., Hasegawa, S. and Hirano, T. 1994. Development of mitochondrion-rich cells in the yolk-sac membrane of embryos and larvae of tilapia, Oreochromis mossambicus, in fresh water and seawater. J. Exp. Zool. 270: 129–135.
Battaglini, P., Andreozzi, G., Antonucci, R., Aroamone, N., Giro-lamo, P.D., Ferrara, L. and Gargiulo, G. 1993. The effects of cadmium on the gills of the goldfish Carassius auratus L.: metal uptake and histochemical changes. Comp. Biochem. Physiol. 104: 239–247.
Benoit, D.A., Leonhard, E.N., Christensen, G.M. and Fiandt, J.T. 1976. Toxic effects of cadmium on three generations of brook trout (Salvelinus fontinalis). Trans. Am. Fish. Soc. 105: 550–560.
Bentley, P.J. 1992. Influx of zinc by channel catfish (Ictalurus punctatus): uptake from external environment solutions. Comp. Biochem. Physiol. 101C: 215–217.
Bishop, W.E. and McIntosh, A.W. 1981. Acute lethality and effects of sublethal cadmium exposure on ventilation frequency and cough rate of bluegill (Lepomus macrochirus). Arch. Environ. Contam. Toxicol. 10: 519–530.
Brown, M.W., Thomas, D.G., Shurben, D., Solbe, J.F., Kay, J. and Cryer, A. 1986. A comparison of the differential accumulation of cadmium in the tissues of three species of freshwater fish, Salmo gairdneri, Rutilus rutilus and Noemacheilus barbatulus. Comp. Biochem. Physiol. 84C: 213–217.
Fu, H. and Lock, R.A.C. 1990. Pituitary response to cadmium during the early development of tilapia (Oreochromis mos-sambicus). Aquat. Toxicol. 16: 9–18.
Fu, H., Lock, R.A.C. and Wendelaar Bonga, S.E. 1989. Effect of cadmium on prolactin cell activity and plasma electrolytes in the freshwater teleost Oreochromis mossambicus. Aquat. Toxicol. 14: 295–306.
Giles, M.A. 1984. Electrolyte and water balance in plasma and urine of rainbow trout (Salmo gairdneri) during chronic exposure to cadmium. Can. J. Fish. Aquat. Sci. 41: 1678–1685.
Gill, T.S., Tewari, H. and Pande, J. 1990. In vivo and in vitro effects of cadmium on selected enzymes in different organs of the fish Barbus conchonius Ham. (rosy barb). Comp. Biochem. Physiol. 101C: 519–523.
Goss, G.G. and Wood, C.M. 1990. Na+ and Cl- uptake kinetics, diffusive effluxes and acidic equivalent fluxes across the gills of rainbow trout. 152: 521–547.
Guggino, W.B. 1980. Salt balance in embryos of Fundulus heteroclitus and F. bermudae adapted to sea water. Am. J. Physiol. 238: R42–49.
Hayes, F.R., Darcy, D.A. and Sullivan, C.M. 1946. Changes in the inorganic constituents of developing salmon eggs. J. Biol. Chem. 163: 621–631.
Heath, A.G. 1987. Osmotic and ionic regulation. In Water Pollution and Fish Physiology. pp. 107–130. Edited by A.G. Heath. CRC Press, Boca Raton.
Hobe, H., Laurent, P. and McMahon, B.R. 1984. Whole body calcium flux rates in freshwater teleosts as a function of ambient calcium pH levels: a comparison between the euryhaline trout, Salmo gairdneri and stenohaline bullhead, Ictalurus nebulosus. J. Exp. Biol. 113: 237–252.
Hogstrand, C., Reid, S.D. and Wood, C.M. 1995. Ca2+ versus Zn2+ transport in the gills of freshwater rainbow trout and the cost of adaptation to waterborne Zn2+. J. Exp. Biol. 198: 337–348.
Hogstrand, C., Wilson, R.W., Polgar, D. and Wood, C.M. 1994. Effects of zinc on the kinetics of branchial calcium uptake in freshwater rainbow trout during adaptation to waterborne zinc.J. Exp. Biol. 186: 55–73.
Hwang, P.P., Lin, S.W. and Lin, H.C. 1995. Different sensitivities to cadmium in tilapia larvae (Oreochromis mossambicus; Teleostei). Arch. Environ. Contam. Toxicol. 29: 1–7.
Hwang, P.P., Tsai, Y.N. and Tung, Y.C. 1994. Calcium balance in embryos and larvae of the freshwater-adapted teleost, Oreochromis mossambicus. Fish Physiol. Biochem. 13: 325–333.
Hwang, P.P., Tung, Y.C. and Chang, M.H. 1996. Effect of evironmental calcium levels on calcium uptake in tilapia larvae (Oreochromis mossambicus). Fish Physiol. Biochem. 15: 363–370.
Iger, Y., Lock, R.A.C., Meij, J.C.A. and Wendelaar Bonga, S.E. 1994. Effects of water-borne cadmium on the skin of the common carp (Cyprinus carpio). Arch. Eviron. Contam. Toxicol. 26: 342–350.
Kuroshima, R. and Kimura, S. 1990. Changes in toxicity of Cd and its accumulation in girella and goby with their growth. Nippon Suisan Gakkaishi 56: 431–435.
Lauren, D.J. and McDonald, D.G. 1987. Acclimation to copper by rainbow trout, Salmo gairdneri physiology. Can. J. Fish. Aquat. Sci. 44: 99–104.
Laurent, P. and Perry, S.F. 1991. Environmental effects on fish gill morphology. Physiol. Zool. 64: 4–25.
Li, J., Eygensteyn, J., Lock, R.A.C., Verbost, P.M., Van Der Heijden, A.J.H., Wendelaar Bonga, S.E. and Flik, G. 1995. Branchial chloride cells in larvae and juveniles of freshwater tilapia Oreochromis mossambicus. J. Exp. Biol. 198: 2177–2184.
Lee, T.H., Hwang, P.P. and Lin, H.C. 1996. Morphological changes of integumetal chloride cells to ambient cadmium during the early development of the teleost, Oreochromis mossambicus. Environ. Biol. Fish. 45: 95–102.
Majewski, H.S. and Giles, M.A. 1981. Cardiovascular-respiratory responses of rainbow trout (Salmo gairdneri) during chronic exposure to sublethal concentrations of cadmium. Water Res. 15: 1211–1217.
McCarty, L.S. and Houston, A.H. 1976. Effects of exposure to sublethal levels of cadmium upon water-electrolyte status in the goldfish (Carassius auratus). J. Fish Biol. 9: 11–19.
McKim, J.M. and Nichols, J.W. 1994. Use of physiologically based toxicokinetic models in a mechanistic approach to aquatic toxicology. In Aquatic Toxicology: Molecular, Biochemical, and Cellular Perspectives. pp. 369–519. Edited by D.C. Malins and G.K. Ostrander. CRC Press, Boca Raton.
Middaugh, D.P. and Dean, J.M. 1977. Comparative sensitivity of eggs, larvae and adults of the estuarine teleost, Fundulus heteroclitus and Menidia menidia to cadmium. Bull. Environ. Contam. Toxicol. 17: 645–652.
Mukherjee, J.K. and Sinha, G.M. 1993. Cadmium toxicity on haematological and biochemical aspects in an Indian fresh-water major carp, Labeo rohita (Hamilton). J. Freshw. Biol. 5: 245–251.
Payan, P. and Matty, A.J. 1975. The characteristics of ammonia excretion by an isolated perfused head of trout (Salmo gairdneri): effect of temperature and CO2-free Ringer. J. Comp. Physiol. 96: 167–184.
Perry, S.F., Booth, C.E. and McDonald, D.G. 1985. Isolated per-fused head of rainbow trout II: Ionic fluxes. Am. J. Physiol. 249: R255–R261.
Perry, S.F. and Wood, C.M. 1985. Kinetics of branchial calcium uptake in the rainbow trout: effects of acclimation to various external calcium levels. J. Exp. Biol. 116: 411–433.
Pratap, H.B., Fu, H., Lock, R.C.A. and Wendelaar Bonga, S.E. 1989. Effects of waterborne and dietary cadmium on plasma ions of the teleost Oreochromis mossambicus in relation to water calcium levels. Arch. Environ. Contam. Toxicol. 18: 568–575.
Pratap, H.B. and Wendelaar Bonga, S.E. 1990. Effects of water-borne cadmium on plasma cortisol and glucose in the cichlid fish Oreochromis mossambicus. Comp. Biochem. Physiol. 95C: 313–317.
Pratap, H.B. and Wendelaar Bonga, S.E. 1993. Effect of ambient and dietary cadmium on pavement cells, chloride cells, and Na/K-ATPase activity in the gills of the freshwater teleost Oreochromis mossambicus at normal and high calcium levels in the ambient water. Aquat. Toxicol. 26: 133–150.
Rani, A.U. and Ramaurthi, R. 1987. Cadmium induced behavioral abnormalities of the fish Tilapia mossambica. Environ. Ecol. 5: 168–169.
Reid, S.D. and McDonald, D.G. 1988. Effects of cadmium, copper and low pH on ion fluxes in the rainbow trout, Salmo gairdneri. Can. J. Fish. Aquat. Sci. 45: 244–253.
Roch, M. and Maly, E.J. 1979. Relationship of cadmium-induced hypocalcemia with mortality in rainbow trout (Salmo gaird-neri) and the influence of temperature on toxicity. J. Fish. Res. Bd. Can. 36: 1297–1303.
Rombough, P.J. and Garside, E.T. 1982. Cadmium toxicity and accumulation in eggs and alevin of Atlantic salmon, Salmo salar. Can. J. Zool. 60: 2006–2014.
Rombough, P.J. and Garside, E.T. 1984. Disturbed ion balance in alevins of Atlantic salmon, Salmo salar, chronically exposed to sublethal concentrations of cadmium. Can. J. Zool. 62: 1443–1450.
SAS Institute. 1985. SAS User's Guide: Statistics. Version 5. SAS Inst Inc, Cary.
Schoenmakers, T.J.M., Klaren, P.H.M., Flik, G., Lock, R.A.C., Pang, P.K.T. and Wendelaar Bonga, S.E. 1992. Actions of cadmium on basolateral plasma membrane proteins involved in calcium uptake by fish intestine. J. Membr. Biol. 127: 161–172.
Shella, M., Mallika, G. and Muniandy, S. 1995. Impact of cadmium on food utilization, growth and body composition in the fish Oreochromis mossambicus. Environ. Ecol. 13: 410–414.
Shivaraj, K.M. and Patil, H.S. 1988. Toxicity of cadmium and copper to a freshwater fish Puntius arulius. Environ. Ecol. 6: 5–8.
Sovenyi, J. and Szakolcai, J. 1993. Studies on the toxic and immunosuppressive effects of cadmium on the common carp. Acta. Vet. Hung. 41: 415–426.
Spry, D.J. and Wood, C.M. 1989. A kinetic method for the measurement of zinc influx in vivo in the rainbow trout and the effects of waterborne calcium on flux rates. J. Exp. Biol. 142: 425–446.
Swandulla, D. and Armstrong, C.M. 1989. Calcium channel block by cadmium in chicken sensory neurons. Proc. Nat. Acad. Sci. USA 86: 1736–1740.
Verbost, P.M., Flik, G., Lock, R.A.C. and Wendelaar Bonga, S.E. 1987. Cadmium inhibition of Ca 2+ uptake in rainbow trout gills. Am. J. Physiol. 253: R216–R221.
Verbost, P.M., Flik, G., Lock, R.A.C. and Wendelaar Bonga, S.E. 1988. Cadmium inhibits plasma membrane calcium transport. J. Membr. Biol. 102: 97–104.
Verbost, P.M., Rooij, J.V., Flik, G., Lock, R.A.C. and Wendelaar Bonga, S.E. 1989a. Cadmium inhibition of the erythrocyte Ca2+ pump. J. Biol. Chem. 264: 5613–5615.
Verbost, P.M., Rooij, J.V., Flik, G., Lock, R.A.C. and Wendelaar Bonga, S.E. 1989b. The movement of cadmium through freshwater trout branchial epithelium and its interference with calcium transport. J. Exp. Biol. 145: 185–197.
Wood, C.M. 1992. Flux measurements as indices of H+ and metal effects on freshwater fish. Aquat. Toxicol. 22: 239–264.
Wright, D.A., Meteyer, M.J. and Martin, F.D. 1985. Effects of calcium on cadmium uptake and toxicity in larvae and juveniles of striped bass (Morone saxatilis). Bull. Environ. Contam. Toxicol. 34: 196–204.
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Chang, MH., Lin, HC. & Hwang, P. Effects of cadmium on the kinetics of calcium uptake in developing tilapia larvae, Oreochromis mossambicus. Fish Physiology and Biochemistry 16, 459–470 (1997). https://doi.org/10.1023/A:1007780602426
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DOI: https://doi.org/10.1023/A:1007780602426