Osmoregulation in elasmobranchs: A review for fish biologists, behaviourists and ecologists

Marine and Freshwater Behaviour and Physiology

Volumn 39, Issue 3, 2006, Pages 209-228

  Hammerschlag, Neil ^a,b  

^a UNIVERSITY OF MIAMI   (United States)

^b ReefQuest Centre for Shark Research   (Canada)

Author keywords

Elasmobranch; Gill; Osmoregulation; Rectal gland; Shark; Urea

Indexed keywords

FISH BIOLOGY; OSMOREGULATION; SHARK; UREA;

ELASMOBRANCHII;

EID: 33747691734     PISSN: 10236244     EISSN: 10290362     Source Type: Journal    
DOI: 10.1080/10236240600815820     Document Type: Review

References (99)

1. Anderson, PM. (1980) Glutamine and N-acetylglutamate-dependent carbamoyl phosphate synthetase in elasmobranchs Science, 208, pp. 291-293.
2. Anderson, PM.(1995) Urea cycle in fish: Molecular and mitochondrial studies. In Ionoregulation: Cellular and molecular approaches to fish ionic regulation. (pp. 57-83). New York: Academic Press. Fish Physiology
3. Anderson, PM.(2001) Urea and glutamine synthesis: Environmental influences on nitrogen excretion. In Nitrogen excretion. (pp. 239-278). San Diego: Academic Press. Fish Physiology
4. Anderson, WG and Good, JP and Franklin, CE and Hazon, N. (2003) Scaling of rectal gland mass in the European lesser-spotted dogfish J. Fish Biol., 62, pp. 749-751.
5. Anderson, WG and Good, JP and Pillans, RD and Hazon, N and Franklin, CE. (2005) Hepatic urea biosynthesis in the euryhaline elasmobranch Carcharhinus leucas J. Exp. Zool., 303, pp. 917-921.
6. Anderson, WG and Takei, Y and Hazon, N. (2002) Osmotic and volaemic effects on drinking rate in elasmobranch fish J. Exp. Biol., 205, pp. 1115-1122.
7. Armour, KJ and O'Toole, LB and Hazon, N. (1993) The effects of dietary protein restriction on the secretory dynamics of 1 α-hydroxycorticosterone and urea in the dogfish, Scyliorhinus canicula: A possible role for 1 α-hydroxycorticosterone in sodium retention J. Endo., 138, pp. 275-282.
8. Blanco, G and Mercer, RW. (1998) Isozymes of the Na-K-ATPase: Heterogeneity in structure, diversity in function Am. J. Physiol., 275, pp. F633-650.
9. Boyd, TA and Cha, CJ and Forster, RP and Goldstein, L. (1977) Free amino acids in tissues of the skate Raja erinacea and the stingray Dasyatis sabina: Effects of environmental dilution J. Exp. Zool., 199, pp. 435-442.
10. Boylan, JW.(1967) Gill permeability in Squalus acanthias. In Sharks, skates and rays. (pp. 197-206). Baltimore: Johns Hopkins University Press.
11. Burger, JW. (1965) Roles of the rectal gland and kidneys in salt and water excretion in the spiny dogfish Physiol. Zool., 38, pp. 191-196.
12. Burger, JW and Hess, WN. (1960) Function of the rectal gland in the spiny dogfish Science, 131, pp. 670-671.
13. Compagno LJV.(1990) Shark exploitation and conservation. In Elasmobranchs as living resources: Advances in the biology, ecology, systematics, and the status of the fisheries, Technical report NMFS 90. (pp. 391-414). Washington DC: National Oceanic and Atmospheric Administration.
14. Conte, FP.(1969) Salt secretion. In Fish Physiology. (pp. 241-292). New York: Academic Press.
15. DeBoeck, G and Grosell, M and Wood, CM. (2001) Sensitivity of the spiny dogfish (Squalus acanthias) to waterborne silver exposure Aquat. Toxicol., 54, pp. 261-275.
16. Evans, DH.(1993) Osmotic and Ionic Regulation. In The physiology of fishes. Boca Raton: CRC Press.
17. Evans, DH and Kormanik, GA. (1985) Urea efflux from the Squalus acanthias pup: The effect of stress J. Exp. Biol., 119, pp. 375-379.
18. Evans, DH and Piermarini, PM and Choe, KP.(2004) Homeostasis: Osmoregulation, pH regulation, and nitrogen excretion. In Biology of sharks and their relatives. Boca Raton: CRC Press.
19. Evans, DH and Piermarini, PM and Choe, KP. (2005) The multifunctional fish gill: Dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste Physiol. Rev., 85, pp. 97-177.
20. Evans, DH and Piermarini, PM and Potts, WTW. (1999) Ionic transport in the fish gill epithelium J. Exp. Zool., 283, pp. 641-652.
21. Fines, GA and Ballantyne, JS and Wright, PA. (2001) Active urea transport and an unusual basolateral membrane composition in the gills of a marine elasmobranch Am. J. Physiol., 280, pp. R16-R24.
22. Forster, RP and Goldstein, L. (1976) Intracellular osmoregulatory role of amino acids and urea in marine elasmobranchs Am. J. Physiol., 230, pp. 925-931.
23. Friedman, PA and Hebert, SC. (1990) Diluting segment in kidney of dogfish shark I. Localization and characterization of chloride absorption Am. J. Physiol., 258, pp. R398-408.
24. Gelsleichter, J.(2004) Hormonal regulation of elasmobranch physiology. In Biology of sharks and their relatives. (pp. 287-324). Boca Raton: CRC Press.
25. Gerst, JW and Thorson, TB. (1977) Effects of saline acclimation on plasma electrolytes, urea excretion, and hepatic urea biosynthesis in a freshwater stingray, Potamotrygon sp. Garman, 1877 Comp. Biochem. Physiol. A., 56, pp. 87-93.
26. Goldstein, L and Forster, RP. (1971a) Urea biosynthesis and excretion in freshwater and marine elasmobranchs Comp. Biochem. Physiol. B., 39, pp. 415-421.
27. Goldstein, L and Forster, RP. (1971b) Osmoregulation and urea metabolism in the little skate Raja erinacea Am. J. Physiol. 220, pp. 742-746.
28. Goldstein, L and Oppelt, WW and Maren, TH. (1968) Osmotic regulation and urea metabolism in the lemon shark Negaprion brevirostris Am. J. Physiol., 215, pp. 1493-1497.
29. Goldstein, L and Perlman, DF.(1995) Nitrogen metabolism, excretion, osmoregulation, and cell volume regulation. In Nitrogen metabolism and excretion. (pp. 91-104). Boca Raton: CRC press.
30. Griffith, RW and Pang, PKT and Srivastava, AK and Pickford, GE. (1973) Serum composition of freshwater stingrays (Potamotrygonidae) adapted to fresh and dilute sea water Biol. Bull., 144, pp. 304-420.
31. Grimes, DJ and Brayton, P and Colwell, RR and Gruber, SH. (1985) Vibrios as autochthonous flora of neritic sharks Syst. Appl. Microbiol., 6, pp. 221-226.
32. Hays, RM and Levine, SD and Myers, JD and Heinermann, HO and Kaplan, MA and Franki, N and Berliner, H. (1977) Urea transport in the dogfish kidney J. Exp. Zool., 199, pp. 309-316.
33. Haywood, GP. (1973) Hypo-osmotic regulation coupled with reduced metabolic urea in the dogfish Poroderma africanum: An analysis of serum osmolarity, chloride, and urea Mar. Biol., 23, pp. 121-127.
34. Haywood, GP. (1975) Indications of sodium, chloride, and water exchange across the gills of the striped dogfish Poroderma africanum Mar. Biol., 29, pp. 267-276.
35. Hazon, N and Henderson, IW. (1984) Secretory dynamics of l α-hydroxycorticosterone in the elasmobranch fish, Scyliorhinus canicula J. Endocrinol., 103, pp. 205-211.
36. Hazon, N and Wells, A and Pillans, RD and Good, JP and Anderson, WG and Franklin, CE. (2003) Urea based osmoregulation and endocrine control in elasmobranch fish with special reference to euryhalinity Comp. Biochem. Physiol. B., 136, pp. 685-700.
37. Hill, WG and Mathai, JC and Gensure, RH and Zeidel, JD and Apodaca, G and Saeenz, JP and Kinne-Saffran, E and Kinne, R and Zeidel, M. (2004) Permeabilities of teleosts and elasmobranch gill apical membranes: Evidence that lipid bilayers alone do not account for barrier function Am. J. Physiol. Cell Physiol., 287, pp. 235-242.
38. Hochachka, PW and Somero, GN.(2002) Biochemical adaptation. Mechanism and process in physiological evolution. Oxford: Oxford University Press.
39. Janech, MG and Fitzgibbon, WR and Chen, R and Nowak, MW and Miller, DH and Paul, RV and Ploth, DW. (2003) Molecular characterization of a urea transporter from the kidney of the Atlantic stingray Am. J. Physiol., 284, pp. F996-1005.
40. Jones, RT and Price, KS, Jr. (1974) Osmotic responses of spiny dogfish (Squalus acanthias L.) embryos to temperature and salinity stress Comp. Biochem. Physiol. A., 47, pp. 971-979.
41. Kempton, RT. (1953) Studies on the elasmobranch kidney. II. Reabsorption of urea by the smooth dogfish, Mustelus canis Biol. Bull., 104, pp. 45-56.
42. King, PA and Goldstein, L. (1983) Organic osmolytes and cell volume regulation in fish Mol. Physiol., 4, pp. 53-66.
43. Knight, IT and Grimes, DJ and Colwell, RR. (1988) Bacterial hydrolysis of urea in the tissues of carcharhinid sharks Can. J. Fish. Aquat. Sci., 45, pp. 357-360.
44. Lacy, ER and Reale, E. (1991) Fine structure of the elasmobranch renal tubule: Intermediate, distal and collecting duct segments of the little skate Am. J. Anat., 192, pp. 478-497.
45. MacKenzie, S and Cutler, CP and Hazon, N and Cramb, G. (2002) The effects of dietary sodium loading on the activity and expression of Na, K-ATPase in the rectal gland of the European dogfish (Scyliorhinus canicula) Comp. Biochem. Physiol. B., 131, pp. 185-200.
46. Mangum, CP and Haswell, MS and Johansen, K and Towle, DW. (1978) Inorganic ions and pH in the body fluids of Amazon animals Can. J. Zool., 56, pp. 907-916.
47. Marshall, WS and Bryson, SE. (1998) Transport mechanisms of seawater teleost chloride cells: An inclusive model of a multifunctional cell Comp. Biochem. Physiol. A., 119, pp. 97-106.
48. Martin, RA. (2005) Conservation of freshwater and euryhaline elasmobranchs: A review J. Mar. Biol. Assoc. UK., 85, pp. 1049-1073.
49. +-ATPase and chloride cell function. In Cellular and molecular approaches to fish ionic regulation. (pp. 285-315). San Diego: Academic Press. Fish Physiology
50. Mommsen, TP and Wash, PJ. (1989) Evolution of urea synthesis in vertebrates: The piscine connection Science, 243, pp. 72-75.
51. Mommsen, TP and Walsh, PJ.(1991) Urea synthesis in fishes: Evolutionary and biochemical perspectives. In Biochemistry and molecular biology of fishes. (pp. 137-163). New York: Elsevier.
52. Morgan, RL and Ballantyne, JS and Wright, PA. (2003a) Regulation of a renal urea transporter with reduced salinity in a marine elasmobranch, Raja erinacea J. Exp. Biol., 206, pp. 3285-3292.
53. Morgan, RL and Wright, PA and Ballantyne, JS. (2003b) Urea transport in kidney brush-border membrane vesicles from an elasmobranch, Raja erinacea J. Exp. Biol., 206, pp. 3293-3302.
54. Mouritsen, OG and Jorgensen, K. (1994) Dynamic order and disorder in lipid bilayers Chem. Phys. Lipids, 73, pp. 3-25.
55. Oguri, M. (1964) Rectal glands of marine and fresh-water sharks: Comparative histology Science, 144, pp. 1151-1152.
56. Part, P and Wright, PA and Wood, CM. (1998) Urea and water permeability in dogfish (Squalus acanthias) gills Comp. Biochem. Physiol., 119, pp. 117-123.
57. Payan, P and Goldstein, L and Forster, RP. (1973) Gills and kidneys in ureosmotic regulation in euryhaline skates Am. J. Physiol., 224, pp. 367-372.
58. Perry, SF. (1997) The chloride cell: Structure and function in the gills of freshwater fishes Ann. Rev. Physiol., 59, pp. 325-347.
59. Piermarini, PM and Evans, DH. (1998) Osmoregulation of the Atlantic stingray (Dasyatis sabina) from the freshwater Lake Jesup of the St. Johns River Florida. Physiol. Zool., 71, pp. 553-560.
60. +-ATPase in the gills and rectal gland of a euryhaline elasmobranch (Dasyatis sabina) J. Exp. Biol., 203, pp. 2957-2966.
61. Piermarini, PM and Evans, DH. (2001) Immunochemical analysis of the vacuolar proton-ATPase B-subunit in the gills of a euryhaline stingray (Dasyatis sabina): Effects of salinity and relation to Na/K -ATPase J. Exp. Biol., 204, pp. 3251-3259.
62. Piermarini, PM and Verlander, JW and Royaux, IE and Evans, DH. (2002) Pendrin immunoreactivity in the gill epithelium of a euryhaline elasmobranch Am. J. Physiol Regul. Intergr. Comp. Physiol., 283, pp. 983-992.
63. Pillans, RD and Franklin, CE. (2004) Plasma osmolyte concentrations and rectal gland mass of bull sharks Carcharhius leucus, captured along a salinity gradient Comp. Biochem. Physiol. A., 138, pp. 363-371.
64. + -ATPase activity in gill, rectal gland, kidney and intestine J. Comp. Phyiol. B., 175, pp. 37-44.
65. Poulsen, JM. (1981) Changes in selected blood serum constituents, as a function of salinity variations, in the marine elasmobranch, Sphyrna tiburo Comp. Biochem. Physiol. A., 70, pp. 127-131.
66. Price, KS and Daiber, FC, Jr. (1967) Osmotic environments during fetal development of dogfish, Mustelus canis (Mitchill) and Squalus acanthias (Linnaeus), and some comparisons with skates and rays Physiol. Zool., 40, pp. 248-260.
67. Read, LJ. (1968a) Urea and trimethylamine oxide levels in elasmobranch embryos Biol. Bull., 135, pp. 537-547.
68. Read, LJ. (1968b) Ornithine-urea cycle enzymes in early embryos of the dogfish Squalus sucleyi and the skate Raja binoculata Comp. Bio. Physiol., 24, pp. 669-674.
69. Robertson, JD. (1975) Osmotic constituents of the blood plasma and parietal muscle of Squalus acanthias L. Biol. Bull., 148, pp. 303-319.
70. Robertson, JD. (1976) Chemical composition of the body fluids and muscle of the hagfish Myxine glutinosa and the rabbit-fish Chimaera monstrosa J. Zool. (London)., 178, pp. 261-277.
71. Schmidt-Nielsen, B and Truniger, B and Rabinowitz, L. (1972) Sodium linked urea transport by the renal tubule of the spiny dogfish Squalus acanthias Comp. Biochem. Physiol. A., 42, pp. 13-25.
72. Schooler, JM and Goldstein, L and Hartman, C and Forster, RP. (1966) Pathways of urea synthesis in the elasmobranch, Squalus acanthias Comp. Biochem. Physiol., 18, pp. 271-281.
73. Simpfendorfer, CA and Heupel, MR.(2004) Assessing habitat use and movement. In Biology of sharks and their relatives. (pp. 553-572). Boca Raton: CRC Press.
74. Smith, HW. (1931) The absorption and excretion of water and salts by the elasmobranch fishes. I. Freshwater elasmobranchs Am. J. Physiol., 98, pp. 296-310.
75. Smith, CP and Wright, PA. (1999) Molecular characterization of an elasmobranch urea transporter Am. J. Physiol., 276, pp. R622-626.
76. Steele, SL and Yancey, PH and Wright, PA. (2004) Dogmas and controversies in the handling of nitrogenous wastes: Osmoregulation during early embryonic development in the marine little skate Raja erinacea; response to changes in external salinity J. Exp. Biol., 207, pp. 2021-2031.
77. Steele, SL and Yancey, PH and Wright, PA. (2005) The little skate Raja erinacea exhibits an extrahepatic ornithine urea cycle in the muscle and modulates nitrogen metabolism during low-salinity challenge Physiol. Biochem. Zool., 78, pp. 216-226.
78. Sulikowski, JA and Maginniss, LA. (2001) Effects of environmental dilution on body fluid regulation in the yellow stingray, Urolophus jamaicensis Comp. Biochem. Physiol. A., 128, pp. 223-232.
79. Sundström, LF and Gruber, SH and Clermont, SM and Correia, JPS and de Marignac, JRC and Morrissey, JF and Lowrance, CR and Thomassen, L and Oliveira, MT. (2001) Review of elasmobranch behavioral studies using ultrasonic telemetry with special reference to the lemon shark, Negaprion brevirostris, around Bimini Islands, Bahamas Env. Biol. Fish., 60, pp. 225-250.
80. Tam, WL and Wong, WP and Loong, AM and Hiong, KC and Chew, SF and Ballantyme, JS and Ip, YK. (2003) The osmotic response of the Asian freshwater stingray (Himantura signifer) to increased salinity: A comparison with marine (Potamotrygon motoro) stingrays J. Exp. Biol., 206, pp. 2931-2940.
81. Takei, Y and Loretz, CA.(2005) Endocrinology. In The physiology of fishes. (pp. 271-318). Boca Raton: CRC Press.
82. Thorson, TB. (1961) The partitioning of body water in osteichthyes: Phylogenetic and ecological implications in aquatic vertebrates Biol. Bull., 120, pp. 238-254.
83. Thorson, TB. (1962) Partitioning of body fluids in the Lake Nicaragua shark and three marine sharks Science, 138, pp. 688-690.
84. Thorson, TB. (1970) Freshwater stingrays, Potamotrygon spp: Failure to concentrate urea when exposed to saline medium Life Sci., 9 pp. 893-900.
85. Thorson, TB and Cowan, CM and Watson, DE. (1967) Potamotrygon spp: Elasmobranchs with low urea content Science, 158, pp. 375-377.
86. Thorson, TB and Cowan, CM and Watson, DE. (1973) Body fluid solutes of juveniles and adults of the euryhaline bull shark Carcharhinus leucas from freshwater and saline environments Physiol. Zool., 46, pp. 29-42.
87. Thorson, TB and Gerst, JW. (1972) Comparison of some parameters of serum and uterine fluid of pregnant, viviparious sharks (Carcharhinus leucas) and serum of their near-term young Comp. Biochem. Physiol. A., 42, pp. 33-40.
88. Thorson, TB and Wotton, RM and Georgi, TA. (1978) Rectal gland of freshwater stingrays, Potamotrygon spp. (Chondrichthyes: Potamotrgonidae) Biol. Bull., 154, pp. 508-516.
89. + -ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias) J. Exp. Biol., 208, pp. 345-354.
90. Urist, MR. (1962) Calcium and other ions in blood and skeleton of Nicaraguan fresh-water shark Science, 137, pp. 984-986.
91. Walsh, PJ and Mommsen, TP.(2001) Evolutionary considerations of nitrogen metabolism and excretion. In Nitrogen excretion. (pp. 1-30). San Diego: Academic Press. Fish Physiology
92. Walsh, PJ and Smith, CP.(2001) Urea transport. In Nitrogen excretion. (pp. 279-307). San Diego: Academic Press.
93. Wilkie, MP. (2002) Ammonia excretion and urea handling by fish gills: Present understanding and future research challenges J. Exp. Zool., 293, pp. 284-301.
94. Wilson, JM and Morgan, JD and Vogal, AW and Randall, DJ. (2002) Branchial mitochondria-rich cells in the dogfish Squalus acanthias Comp. Biochem. Physiol. A., 132, pp. 365-374.
95. Wilson, JM and Randall, DJ and Vogal, AW and Iwama, GK. (1997) Immunolocalization of proton-ATPase in the gills of the elasmobranch, Squalus acanthias J. Exp. Zool., 278, pp. 78-86.
96. Wong, TM and Chan, DKO. (1977) 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, pp. 85-96.
97. Wood, CM.(1993) Ammonia and urea metabolism and excretion. In The physiology of fishes. (pp. 379-425). Boca Raton: CRC Press.
98. Wood, CM and Matsuo, AYO and Gonzalez, RJ and Wilson, RW and Patrick, ML and Val, AL. (2002) Mechanisms of ion transport in Potamotrygon, a stenohaline freshwater elasmobranch native to the ion-poor blackwater of the Rio Negro J. Exp. Biol., 205, pp. 3039-3054.
99. Wood, CM and Part, P and Wright, PA. (1995) Ammonia and urea metabolism in relation to gill function and acid-base balance in a marine elasmobranch, the spiny dogfish (Squalus acanthias) J. Exp. Biol., 198, pp. 1545-1558.