Abstract
Winter skates, Leucoraja ocellata, exposed to 80% and 50% seawater (SW) exhibited rapid and significant weight gains followed by a slight recovery to new steady state levels within 8 days. Skates were acclimated at each salinity (100% SW [N = 16], 80% SW [N = 8], 50% SW [N = 8]), anesthetized (MS222) and bled from the caudal vein. In 100% SW, skate plasma (930 mOsm/kg) was slightly hyperosmotic to the external medium (922 mOsm/kg). Plasma osmolality decreased with seawater dilution, but became increasingly hyperosmotic to the bathing media. The environmental dilutions resulted in significant, but disproportionate changes in plasma Cl−, P−, Na+, Ca+, Mg+, trimethylamine oxide (TMAO) and urea concentrations. Mean corpuscular [Hb] and milliliter RBC water measurements suggest that skate red cells swelled less at each dilution than predicted for a passive erythrocyte osmometer. Concentrations of the major RBC solutes K+, urea, TMAO and Cl− decreased by 8, 25, 5 and 21%, respectively in 80% SW. In 50% SW, K+, urea, TMAO and Cl− concentrations decreased by 9, 47, 36 and 15%, respectively. Quantitatively, the other measured intracellular electrolytes (Mg+, Na+, P− and Ca+) also exhibited disproportionate changes in concentration. Our results indicate that L. ocellata is a euryhaline elasmobranch that can tolerate significant reduction in the external salinity through the release of both ions and urea from the extracellular compartments while retaining electrolytes at the expense of urea in the intracellular compartment.
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References cited
Bigelow, H.B. & W.C. Schroeder. 1953. Fishes of the Gulf of Maine. Fish. Bull. 53: 63-65.
Boyd, T.A., C.J. Cha, R.P. Forster & L. Goldstein. 1977. Free amino acids in tissues of the little skate, Raja erinacea, and the stingray, Dasyatis sabina: Effects of environmental dilution. J. Exp. Zool. 199: 435-442.
Carlson, S.R. & L. Goldstein. 1997. Urea transport across the cell membrane of skate erythrocytes. J. Exp. Zool. 277: 275-282.
Chan, D.K.O. & T.M. Wong. 1977a. Physiological adjustments to dilution of the external medium in the lip-shark Hemiscyllium plagiosum (Bennett). I. Size of body compartments and osmolyte composition. J. Exp. Zool. 200: 71-84.
Chan, D.K.O. & T.M. Wong. 1977b. Physiological adjustments to dilution of the external medium in the lip-shark Hemiscyllium plagiosum (Bennett). II. Branchial, renal and rectal gland function. J. Exp. Zool. 200: 85-95.
Cohen, J.J., M.A. Krupp & C.A. Chidsey III. 1958. Renal conservation of trimethylamine oxide by the spiny dogfish, Squalus acanthias. Am. J. Physiol. 194: 229-235.
Cooper, R.A. & S. Morris. 1998. Osmotic and haemotological response of the Port Jackson shark, Heterodontus portusjacksoni, and the common stingaree, Trygonoptera testacea, upon exposure to diluted sea water. Mar. Biol. 132: 29-42.
De Vlaming, V.L. & M. Sage. 1973. Osmoregulation in the euryhaline elasmobranch, Dasyatis sabina. Comp. Biochem. Physiol. 45A: 31-44.
Forster, R. & L. Goldstein. 1976. Intracellular osmoregulatory role of amino acids and urea in marine elasmobranchs. Am. J. Physiol. 230: 925-931.
Goldstein, L. 1989. Volume regulation in the erythrocyte of the little skate, Raja erinacea. J. Exp. Zool. 2: 136-142.
Goldstein, L. & R. Forster. 1971. Osmoregulation and urea metabolism in the little skate, Raja erinacea. Am. J. Phys. 220(3): 742-746.
Goldstein, L., W.W. Oppelt & T.H. Maren. 1968. Osmotic regulation and urea metabolism in the lemon shark, Negaprion brevirostris. Am. J. Phys. 215(6): 1493-1497.
Haywood, G.P. 1973. Hypo-osmotic regulation coupled with reduced metabolic urea in the dogfish, Poroderma africanum: An analysis of serum osmolality, chloride and urea. Mar. Biol. 23: 121-127.
Holmes, W.N. & E.M. Donaldson. 1969. The body compartments and the distribution of Electrolytes. pp. 1-89. In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, vol. 1, Excretion, Ionic Regulation, Metabolism, Academic Press, New York.
Kaplan, M.A., L. Hays & R.M. Hays. 1974. Evolution of a facilitated diffusion pathway for amides in the erythrocyte. Am. J. Physiol. 226: 1327-1332.
King, P.A. & L. Goldstein. 1983. Organic osmolytes and cell volume regulation in fish. Molec. Physiol. 4: 53-66.
Maginniss, L.A. & M.H. Hitzig. 1987. Acid-base status and electrolytes in red blood cells and plasma of turtles submerged at 3?C. Am J. Physiol. 253: R64-R70.
Pang, P.K.T., R.W. Griffith & J.W. Atz. 1977. Osmoregulation in elasmobranchs. Am. Zool. 17: 365-377.
Piermarini, P.M. & D.H. Evans. 1998. Osmoregulation of the Atlantic stingray (Dasyatis sabina) from the freshwater lake Jesup of the St. Johns River, Florida. Physiol. Zool. 71(5): 553-560.
Rabinowitz, L. & R.A. Gunther. 1973. Urea transport in elasmobranch erythrocytes. Am. J Physiol. 224: 1109-1115.
Robertson, J.D. 1989. Osmotic constituents of the blood plasma and parietal muscle of Scyliorhinus canicula. Comp. Biochem. Physiol. 93A: 799-805.
Semple, R.E., D. Sigsworth & J.T. Stitt. 1970. Seasonal observations on the plasma, red cell and blood volumes of two turtle species native to Ontario. Can. Journ. Physiol Pharm. 48: 282-290.
Shuttleworth, T.J. 1988. Salt andwater balance-extrarenal mechanisms. pp. 171-194. In: T.J. Shuttleworth (ed.) The Physiology of Elasmobranch Fishes, Springer-Verlag.
Scholnick, D.A. & C.P. Magnum. 1991. Sensitivity of hemoglobins to intracellular effectors: Primitive and derived features. J. Exp. Zool. 259: 32-42.
Sulikowski, J.A. & L.A. Maginniss. 2001. Effects of environmental dilution on body fluid regulation in the yellow stingray, Urolophus jamaicensis. Comp. Biochem. Physiol. 128(2): 223-232.
Walsh, P.J., C.M. Wood, S.F. Perry & S. Thomas. 1994. Urea transport by hepatocytes and red blood cells of selected elasmobranch and teleost fish. J. Exp. Biol. 193: 321-335.
Weber, R.E. 1983. TMAO-independence of oxygen affinity and its urea and ATP sensitivities in elasmobranch hemoglobin. J. Exp. Zool. 228: 551-554.
Weckell, J.C. & H. Barnett. 1991. New method for analysis of trimethylamine oxide using ferrous sulfate and EDTA. J. Food Sci. 56: 132-138.
Yancey, P.H & G.N. Somero. 1979. Counteraction of urea destabilization of protein structure by methylamine osmoregulatory solutes of elasmobranch fishes. J. Biochem. 183: 317-323.
Yancey, P.H & G.N. Somero. 1980. Methylamine osmoregulatory solutes of elasmobranch fishes counteract urea inhibition of enzymes. J. Exp. Zool. 212: 205-213.
Yancey, P.H., M.E. Clark, S.C. Hand, R.D. Bowlus & G.N. Somero. 1982. Living with water stress: Evolution of osmolyte systems. Science 217: 214-122
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Sulikowski, J.A., Treberg, J.R. & Howell, W.H. Fluid Regulation and Physiological Adjustments in the Winter Skate, Leucoraja ocellata, Following Exposure to Reduced Environmental Salinities. Environmental Biology of Fishes 66, 339–348 (2003). https://doi.org/10.1023/A:1023918231020
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DOI: https://doi.org/10.1023/A:1023918231020