Freshwater elasmobranchs: A review of their physiology and biochemistry

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 180, Issue 4, 2010, Pages 475-493

  Ballantyne, James S ^a   Robinson, J W ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Elasmobranch; Freshwater; Metabolism; Osmoregulation; Physiology; Salinity

Indexed keywords

AMINO ACID; FRESH WATER; UREA;

ADAPTATION; ANIMAL; BLOOD; CARBOHYDRATE METABOLISM; ELASMOBRANCHII; ELECTROLYTE BALANCE; EVOLUTION; GILL; KIDNEY; LIPID METABOLISM; METABOLISM; OXYGEN CONSUMPTION; PHYSIOLOGY; REPRODUCTION; REVIEW; SALINITY; SALT GLAND; SPECIES DIFFERENCE;

ADAPTATION, BIOLOGICAL; AMINO ACIDS; ANIMALS; CARBOHYDRATE METABOLISM; ELASMOBRANCHII; EVOLUTION; FRESH WATER; GILLS; KIDNEY; LIPID METABOLISM; OXYGEN CONSUMPTION; REPRODUCTION; SALINITY; SALT GLAND; SPECIES SPECIFICITY; UREA; WATER-ELECTROLYTE BALANCE;

DASYATIDAE; ELASMOBRANCHII; POTAMOTRYGONIDAE; TELEOSTEI;

EID: 77952493534     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-010-0447-0     Document Type: Review

References (199)

1. Acher R, Chauvet J, Chauvet M, Rouille Y (1999) Unique evolution of neurohypophysial hormones in cartilaginous fishes: possible implications for urea-based osmoregulation. J Exp Zool 284: 475-484.
2. Anderson WG, Hyodo S, Tsukada T, Meischke L, Pillans RD, Good JP, Takei Y, Cramb G, Franklin CE, Hazon N (2005) Sequence, circulating levels, and expression of C-type natriuretic peptide in a euryhaline elasmobranch, Carcharhinus leucas. Gen Comp Endocrinol 144: 90-98.
3. Anderson WG, Pillans RD, Hyodo S, Tsukada T, Good JP, Takei Y, Franklin CE, Hazon N (2006) The effects of freshwater to seawater transfer on circulating levels of angiotensin II, C-type natriuretic peptide and arginine vasotocin in the euryhaline elasmobranch, Carcharhinus leucas. Gen Comp Endocrinol 147: 39-46.
4. Anderson WG, Taylor JR, Good JP, Hazon N, Grosell M (2007) Body fluid volume regulation in elasmobranch fish. Comp Biochem Physiol 148A: 3-13.
5. Anderson G, Taylor JR, Grosell M, Weihrauch D (2009) Waste not want not-intestinal handling of solutes and water in elasmobranchs. Comp Biochem Physiol 153A: S65.
6. Armour KJ, O'Toole LB, Hazon N (1993) The effect of dietary protein restriction on the secretory dynamics of 1alpha-hydroxycorticosterone and urea in the dogfish, Scyliorhinus canicula: a possible role for 1alpha-hydroxycorticosterone in sodium retention. J Endocrinol 138: 275-282.
7. Ballantyne JS (1997) Jaws, the inside story. The metabolism of elasmobranch fishes. Comp Biochem Physiol 118B: 703-742.
8. Ballantyne JS, Moon TW (1986) Solute effects on mitochondria from an elasmobranch (Raja erinacea) and teleost (Pseudopleuronectes americanus). J Exp Zool 239: 319-328.
9. Ballantyne JS, Moyes CD, Moon TW (1986) Osmolarity affects oxidation of sarcosine by isolated hepatocytes and mitochondria from a euryhaline elasmobranch. J Exp Zool 238: 267-271.
10. Ballatori N, Boyer JL (1988) Characteristics of l-alanine uptake in freshly isolated hepatocytes of the elasmobranch Raja erinacea. Am J Physiol 254: R801-R808.
11. Barboza PS, Farley SD, Robbins CT (1997) Whole-body urea cycling and protein turnover during hyperphagia and dormancy in growing bears (Ursus americanus and U. arctos). Can J Zool 75: 2129-2136.
12. Bittner A, Lang S (1980) Some aspects of the osmoregulation of Amazonian freshwater stingrays (Potamotrygon hystrix)-I. Serum osmolality, sodium and chloride content, water content, hematocrit and urea level. Comp Biochem Physiol 67A: 9-13.
13. Bonaventura J, Bonaventura C, Sullivan B (1974) Urea tolerance as a molecular adaptation of elasmobranch hemoglobins. Science 186: 57-59.
14. Boylan JW (1967) Gill permeability in Squalus acanthias. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates and rays. The Johns Hopkins University Press, Baltimore, pp 197-206.
15. Boylan JW, Feldman B, Antowiak D (1963) Factors affecting gill permeability in Squalus acanthias. Bull Mount Desert Island Biol Lab 5: 29.
16. Brooks DR, Thorson TB, Mayes MA (1981) Fresh-water stingrays (Potamotrygonidae) and their helminth parasites: testing hypotheses of evolution and coevolution. In: Funk VA, Brooks DR (eds) Advances in cladistics. New York Botanical Garden, New York, pp 147-175.
17. Cain DK, Harms CA, Segars A (2004) Plasma biochemistry reference values of wild-caught southern stingrays (Dasyatis americana). J Zoo Wildl Med 35: 471-476.
18. + exchange in the teleost and the elasmobranch. J Exp Zool 239: 183-195.
19. Carrier JC, Evans DH (1972) Ion, water and urea turnover rates in the nurse shark, Ginglymostoma cirratum. Comp Biochem Physiol 41A: 761-764.
20. Carrier JC, Evans DH (1973) Ion and water turnover in the fresh-water elasmobranch Potamotrygon sp. Comp Biochem Physiol 45A: 667-670.
21. Chamberlin ME, Ballantyne JS (1992) Glutamine metabolism in elasmobranch and agnathan muscle. J Exp Zool 264: 269-272.
22. Charvet-Almeida P, Goes de Araujo ML, de Almeida MP (2005) Reproductive aspects of freshwater stingrays (Chondrichthyes: Potamotrygonidae) in the Brazilian Amazon Basin. J Northwest Atl Fish Sci 35: 165-171.
23. Chatchavalvanich K, Thongpan A, Nakai M (2005) Structure of the testis and genital duct of freshwater stingray Himantura signifer (Elasmobranchii: Myliobatiformes: Dasyatidae). Ichthyol Res 52: 123-131.
24. Chew SF, Poothodiyil NK, Wong WP, Ip YK (2006) Exposure to brackish water, upon feeding, leads to enhanced conservation of nitrogen and increased urea synthesis and retention in Asian freshwater stingray Himantura signifer. J Exp Biol 209: 484-492.
25. Choe KP, Evans DH (2003) Compensation for hypercapnia by a euryhaline elasmobranch: effect of salinity and roles of gills and kidneys in freshwater. J Exp Zool 297A: 52-63.
26. +-ATPase in the Atlantic stingray, Dasyatis sabina: primary sequence and expression in the gills. Am J Physiol 287: R981-R991.
27. + absorption in euryhaline elasmobranchs exists in the gills of a stenohaline marine elasmobranch, Squalus acanthias. Comp Biochem Physiol 146A: 155-162.
28. Coelho R, Erzini K (2006) Reproductive aspects of the undulate ray, Raja undulata, from the south coast of Portugal. Fish Res 81: 80-85.
29. Cohen DM (1970) How many recent fishes are there? Proc Calif Acad Sci 38: 341-346.
30. Cohen JJ, Krupp MA, Chidsey CA (1958) Renal conservation of trimethylamine oxide by the spiny dogfish, Squalus acanthias. Am J Physiol 194: 229-235.
31. Compagno LJV (1995) The exploitation and conservation of freshwater elasmobranchs: status of taxa and prospects for the future. J Aquaric Aquat Sci 7: 62-90.
32. Cooper AR (2004) Osmotic, sodium, carbon dioxide and acid-base state of the Port Jackson shark, Heterodontus portusjacksoni, in response to lowered salinity. J Comp Physiol 174B: 211-222.
33. Cooper AR, Morris S (1998a) Osmotic, ionic and haematological response of the Port Jackson shark Heterodontus portusjacksoni and the common stingaree Trygonoptera testacea upon exposure to diluted seawater. Mar Biol 132: 29-42.
34. Cooper AR, Morris S (1998b) The blood respiratory, haematological, acid-base and ionic status of Port Jackson shark, Heterodontus portusjacksoni, during recovery from anesthesia and surgery: a comparison with sampling by direct caudal puncture. Comp Biochem Physiol 119A: 895-903.
35. Cooper AR, Morris S (2004) Haemoglobin function and respiratory status of the Port Jackson shark, Heterodontus portusjacksoni, in response to lowered salinity. J Comp Physiol 174B: 223-236.
36. Cutler CP, Cramb G (2009) Immunohistochemical localization and expression of aquaporin water channel membrane transport protein homologues in the osmoregulatory tissues of the dogfish (Squalus acanthias). Comp Biochem Physiol 153A: S65-S66.
37. De Almeida-Val VMF, Val AL (1993) Evolutionary trends of LDH isozymes in fishes. Comp Biochem Physiol 105B: 21-28.
38. de Vlaming VL, Sage M (1973) Osmoregulation in the euryhaline elasmobranch, Dasyatis sabina. Comp Biochem Physiol 45A: 31-44.
39. Dowd WW, Wood CM, Kajimura M, Walsh PJ, Kultz D (2008) Natural feeding influences protein expression in the dogfish shark rectal gland: a proteomic analysis. Comp Biochem Physiol 3D: 118-127.
40. Dowd WW, Harris BN, Cech JJ, Kuma K (2010) Proteomic and physiological responses of leopard sharks (Triakis semifasciata) to salinity change. J Exp Biol 213: 210-224.
41. Driedzic WR, De Almeida-Val VMF (1996) Enzymes of cardiac energy metabolism in Amazonian teleosts and the fresh-water stingray (Potamotrygon hystrix). J Exp Zool 274: 327-333.
42. Epstein FH, Stoff JS, Silva P (1983) Mechanism and control of hyperosmotic NaCl-rich secretion by the rectal gland of Squalus acanthias. J Exp Biol 106: 25-41.
43. Evans DH (1969) Studies on the permeability to water of selected marine, freshwater and euryhaline teleosts. J Exp Biol 50: 689-703.
44. Evans DH (1981) The egg case of the oviparous elasmobranch Raja erinacea, does osmoregulate. J Exp Biol 92: 337-340.
45. 3- exchange systems evolved before the vertebrates entered freshwater. J Exp Biol 113: 465-469.
46. Evans DH, Piermarini PM, Choe KP (2004) Homeostasis: osmoregulation, pH regulation, and nitrogen excretion. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 247-268.
47. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation and excretion of nitrogenous waste. Physiol Rev 85: 97-177.
48. Fines GA, Ballantyne JS, Wright PA (2001) Active urea transport and an unusual basolateral membrane composition in the gills of a marine elasmobranch. Am J Physiol 280: R16-R24.
49. Forster RP, Goldstein L (1976) Intracellular osmoregulatory role of amino acids and urea in marine elasmobranchs. Am J Physiol 230: 925-931.
50. Forster RP, Hannafin JA, Goldstein L (1978) Osmoregulatory role of amino acids in brain of the elasmobranch, Raja erinacea. Comp Biochem Physiol 60A: 25-30.
51. 14C et d'autres substances a travers la coque de l'ouef de Rousette, Scyliorhinus canicula. C R Acad Sci Paris 290: 427-430.
52. Gelsleichter J (2004) Hormonal regulation of elasmobranch physiology. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 287-323.
53. Gerst JW, 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 56A: 87-93.
54. Goldstein L, Brill SR (1991) Volume-activated taurine efflux from skate erythrocytes: possible band 3 involvement. Am J Physiol 260: R1014-R1020.
55. Goldstein L, Forster RP (1970) Urea biosynthesis and excretion in freshwater and marine elasmobranchs. Bull Mount Desert Island Biol Lab 10: 20-22.
56. Goldstein L, Forster RP (1971a) Osmoregulation and urea metabolism in the little skate Raja erinacea. Am J Physiol 220: 742-746.
57. Goldstein L, Forster RP (1971b) Urea biosynthesis and excretion in freshwater and marine elasmobranchs. Comp Biochem Physiol 39B: 415-421.
58. Goldstein L, Oppelt WW, Maren TH (1968) Osmotic regulation and urea metabolism in the lemon shark Negaprion brevirostris. Am J Physiol 215: 1493-1497.
59. + permeance. J Exp Zool 219: 395-397.
60. Griffith RW, Pang PKT, Srivastava K, Pickford GE (1973) Serum composition of freshwater stringrays (Potamotrygonidae) adapted to freshwater and dilute seawater. Biol Bull 144: 304-320.
61. Hamlett WC (1999) Male reproductive system. In: Hamlett WC (ed) Sharks, skates and rays. The Johns Hopkins University Press, Baltimore, pp 444-447.
62. Hammerschlag N (2006) Osmoregulation in elasmobranchs: a review for fish biologists, behaviourists and ecologists. Mar Freshw Behav Physiol 39: 209-228.
63. Haynes JK, Goldstein L (1993) Volume-regulatory amino acid transport in erythrocytes of the little skate, Raja erinacea. Am J Physiol 265: R173-R179.
64. Haywood GP (1974) The exchangeable ionic space, and salinity effects upon ion, water, and urea turnover rates in the dogfish Poroderma africanum. Mar Biol 26: 69-75.
65. Hazon N, Henderson IW (1984) Secretory dynamics of 1alpha-hydroxycorticosterone in the elasmobranch fish, Scyliorhinus canicula. J Endocrinol 103: 205-211.
66. Hazon N, Tiersch TR, Takei Y (1999) Renin-angiotensin system in elasmobranch fish: a review. J Exp Zool 284: 526-534.
67. Hazon N, Wells A, Pillans RD, Good JP, Anderson WG, Franklin CE (2003) Urea based osmoregulation and endocrine control in elasmobranch fish with special reference to euryhalinity. Comp Biochem Physiol 136B: 685-700.
68. Heffron JK, Moerland TS (2008) Parvalbumin characterization from the euryhaline stingray Dasyatis sabina. Comp Biochem Physiol 150A: 339-346.
69. Helfman GS, Collette BB, Facey DE (1997) The diversity of fishes. Blackwell, Malden.
70. Heupel MR, Simpfendorfer CA (2008) Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquat Biol 1: 277-289.
71. Holmes WN, Donaldson EM (1969) The body compartments and the distribution of electrolytes. In: Hoar WS, Randall DJ (eds) Fish Physiology. Excretion, ionic regulation, and metabolism, vol 1. Academic Press, New York, pp 1-89.
72. Hyodo S, Katoh F, Kaneko T, Takei Y (2004a) A facilitative urea transporter is localized in the renal collecting tubule of the dogfish Triakis scyllia. J Exp Biol 207: 347-356.
73. Hyodo S, Tsukada T, Takei Y (2004b) Neurohypophysial hormones of dogfish, Triakis scyllium: structures and salinity-dependent secretion. Gen Comp Endocrinol 138: 97-104.
74. Idler DR, Truscott B (1967) 1alpha-hydroxycorticosterone: synthesis in vitro and properties of an interrenal steroid in the blood of cartilaginous fish (Genus Raja). Steroids 9: 457-477.
75. Ip YK, Tam WL, Wong WP, Loong AM, Hiong KC, Ballantyne JS, Chew SF (2003) A comparison of the effects of exposure to environmental ammonia on the Asian freshwater stingray Himantura signifer and the Amazonian freshwater stingray Potamotrygon motoro. J Exp Biol 206: 3625-3633.
76. Ip YK, Tam WL, Wong WP, Chew SF (2005) Marine (Taeniura lymma) and freshwater (Himantura signifer) elasmobranchs synthesize urea for osmotic water retention. Physiol Biochem Zool 78: 610-619.
77. Ip YK, Loong AM, Ching B, Tham GHY, Wong WP, Chew SF (2009) The freshwater Amazonian stingray, Potamotrygon motoro, up-regulates glutamine synthetase activity and protein abundance, and accumulates glutamine when exposed to brackish (15‰) water. J Exp Biol 212: 3828-3836.
78. Jampol LM, Epstein FM (1970) Sodium-potassium-activated adenosinetriphosphatase and osmotic regulation by fishes. Am J Physiol 218: 607-611.
79. Janech MG, Piermarini PM (2002) Renal water and solute excretion in the Atlantic stingray in freshwater. J Fish Biology 61: 1053-1057.
80. Janech MG, Fitzgibbon WR, Chen R, Nowak MW, Miller DH, Paul RV, Ploth DW (2003) Molecular and functional characterization of a urea transporter from the kidney of the Atlantic stingray. Am J Physiol 284: F996-F1005.
81. Janech MG, Fitzgibbon WR, Nowak MW, Miller DH, Paul RV, Ploth DW (2006a) Cloning and functional characterization of a second urea transporter from the kidney of the Atlantic stingray, Dasyatis sabina. Am J Physiol 291: R844-R853.
82. Janech MG, Fitzgibbon WR, Ploth DW, Lacy ER, Miller DH (2006b) Effect of low environmental salinity on plasma composition and renal function of the Atlantic stingray, a euryhaline elasmobranch. Am J Physiol 291: F770-F780.
83. Jensen NH (1976) Reproduction of the bull shark, Carcharhinus leucas, in the Lake Nicaragua-Rio San Juan system. In: Thorson TB (ed) Investigations of the Ichthyofauna of Nicaraguan Lakes. School of Life Sciences, University of Nebraska, Lincoln, pp 539-559.
84. Johansen K, Mangum CP, Lykkeboe G (1978) Respiratory properties of the blood of Amazon fishes. Can J Zool 56: 898-906.
85. Johnson MR, Snelson FF (1996) Reproductive life history of the Atlantic stingray Dasyatis sabina (Pisces, Dasyatidae), in the freshwater St. Johns River, Florida. Bull Mar Sci 59: 74-88.
86. Kempton RT (1953) Studies on the elasmobranch kidney. II. Reabsorption of urea by the smooth dogfish, Mustelus canis. Biol Bull 104: 45-56.
87. Kennedy PM, Hume ID (1978) Recycling of urea nitrogen to the gut of the tammar wallaby (Macropus eugenii). Comp Biochem Physiol 61A: 117-121.
88. King PA, Goldstein L (1983a) Organic osmolytes and cell volume regulation in fish. Mol Physiol 4: 53-66.
89. King PA, Goldstein L (1983b) Renal ammoniagenesis and acid excretion in the dogfish, Squalus acanthias. Am J Physiol 245: R581-R589.
90. Kirschner LB (1993) The energetics of osmotic regulation in ureotelic and hypoosmotic fishes. J Exp Zool 267: 19-26.
91. Lacy ER, Reale E (1995) Functional morphology of the elasmobranch nephron and retention of urea. Cellular and molecular approaches to fish ionic regulation. Academic Press Inc, New York, pp 107-146.
92. Lewiston N, Newman A, Robin E, Holtzman D (1979) Shark heart mitochondria: effects of external osmolality on respiration. Science 206: 75-76.
93. Lovejoy NR, Bermingham E, Martin AP (1998) Marine incursion into South America. Nature 396: 421-422.
94. MacKenzie S, Cutler CP, Hazon N, 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 151-152B: 185-200.
95. MacNeil MA, Drouillard KG, Fisk AT (2006) Variable uptake and elimination of stable nitrogen isotopes between tissues in fish. Can J Fish Aquat Sci 63: 345-353.
96. Mandrup-Poulsen J (1981) Changes in selected blood serum constituents, as a function of salinity variations, in the marine elasmobranch, Sphyrna tiburo. Comp Biochem Physiol 70A: 127-131.
97. Mangum CP, Haswell MS, Johansen K (1977) Low salt and high pH in the blood of Amazon fishes. J Exp Zool 200: 163-168.
98. Martin RA (2005) Conservation of freshwater and euryhaline elasmobranchs. J Mar Biol Ass UK 85: 1049-1073.
99. Martin JP, Bonaventura J, Fyhn HJ, Fyhn UEH, Garlick RL, Powers DA (1979) Structural and functional studies of hemoglobins isolated from Amazon stingrays of the genus Potamotrygon. Comp Biochem Physiol 62A: 131-138.
100. McDonald DG, Milligan CL (1992) Chemical properties of the blood. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XIIB. Academic Press, New York, pp 55-133.
101. McGowan DW, Kajiura SM (2009) Electroreception in the euryhaline stingray, Dasyatis sabina. J Exp Biol 212: 1544-1552.
102. Meischke L, Cutler C, Cramb G (2007) Cloning and expression of aquaporin water channels in the euryhaline bull shark, Carcharhinus leucas. Comp Biochem Physiol 146A: S93.
103. Meloni CJ, Cech JJ, Katzman SM (2002) Effect of brackish salinities on oxygen consumption of bat rays (Myliobatis californica). Copeia 2002: 462-465.
104. Morgan RL, Ballantyne JS, Wright PA (2003a) Regulation of a renal urea transport with salinity in a marine elasmobranch Raja erinacea. J Exp Biol 206: 3285-3292.
105. Morgan RL, Ballantyne JS, Wright PA (2003b) Urea transporter in kidney brush-border membrane vesicles from a marine elasmobranch, Raja erinacea. J Exp Biol 206: 3202-3293.
106. Motais R, Isaia J, Rankin JC, Maetz J (1969) Adaptive changes of the water permeability of the teleostean gill epithelium in relation to external salinity. J Exp Biol 51: 529-546.
107. Moyes CD, Moon TW, Ballantyne JS (1986) Osmotic effects on amino acid oxidation in skate liver mitochondria. J Exp Biol 125: 181-195.
108. Mumm DP, Atha DH, Riggs A (1978) The hemoglobin of the common sting-ray Dasyatis sabina: structural and functional properties. Comp Biochem Physiol 60B: 189-193.
109. Musch MW, Goldstein L (1996) High affinity binding of ankyrin induced by volume expansion in skate erythrocytes. J Biol Chem 271: 21221-21225.
110. Musch MW, Koomoa DL, Goldstein L (2004) Hypotonicity-induced exocytosis of the skate anion exchanger skAE1. Role of lipid raft regions. J Biol Chem 279: 39447-39453.
111. Nearing J, Betka M, Quinn S, Hentschel H, Elger M, Baum M, Bai M, Chattopadyhay N, Brown EM, Hebert SC, Harris HW (2002) Polyvalent cation receptor proteins (CaRs) are salinity sensors in fish. Proc Natl Acad Sci USA 99: 9231-9236.
112. Nunez S, Trant JM (1999) Regulation on interrenal gland steroidogenesis in the Atlantic stingray (Dasyatis sabina). J Exp Zool 284: 517-525.
113. Nunez BS, Piermarini PM, Evans AN, Applebaum SL (2005) Cloning and characterization of cDNAs encoding steroidogenic acute regulatory protein from freshwater stingrays (Potamotrygon spp.). J Mol Endocrinol 35: 557-569.
114. Nunez BS, Evans AN, Simpson MA, Wong WP, Ip YK (2006) Characterization of cDNAs encoding cholesterol side chain cleavage and 3-β-hydroxysteroid dehydrogenase in the freshwater stingray Potamotrygon motoro. Comp Biochem Physiol 145B: 306-317.
115. Ogawa M, Hirano T (1982) Studies of the nephron of a freshwater stingray, Potamotrygon magdalenae. Zool Mag 91: 101-105.
116. Oguri M (1964) Rectal glands of marine and fresh-water sharks: comparative histology. Science 144: 1151-1152.
117. Olson KR (1999) Rectal gland and volume homeostasis. In: Hamlett WC (ed) Sharks, skates, and rays. The biology of elasmobranch fishes. The Johns Hopkins University Press, Baltimore, pp 329-352.
118. Otake T, Ishii T, Tanaka S (2005) Otolith strontium: calcium ratios in a freshwater stingray, Himantura signifer Compagno and Roberts, 1982, from the ChaoPhraya River, Thailand. Coast Mar Sci 29: 147-153.
119. Pang PKT, Griffith RW, Atz JW (1977) Osmoregulation in elasmobranchs. Am Zool 17: 365-377.
120. Pang PKT, Furspan PB, Sawyer WH (1983) Evolution of neurohypophyseal hormone actions in vertebrates. Am Zool 23: 655-662.
121. Part P, Wright PA, Wood CM (1998) Urea and water permeability in dogfish (Squalus acanthias) gills. Comp Biochem Physiol 119A: 117-123.
122. Payan P, Maetz J (1971) Balance hydrique chez les elasmobranches: arguments en faveur d'un controle endocrinien. Gen Comp Endocrinol 16: 535-554.
123. 2-free ringer. J Comp Physiol 96: 167-184.
124. Payan P, Goldstein L, Forster RP (1973) Gills and kidneys in ureosmotic regulation in euryhaline skates. Am J Physiol 224: 367-372.
125. Perlman L, Goldstein DF (1988) Nitrogen metabolism. In: Shuttleworth TJ (ed) Physiology of elasmobranch fishes. Springer, New York, pp 253-275.
126. Piermarini PM, Evans DH (1998) Osmoregulation of the Atlantic stingray (Dasyatis sabina) from the freshwater Lake Jesup of the St. Johns River, Florida. Physiol Zool 71: 553-560.
127. +-ATPase in the gills and rectal gland of a euryhaline elasmobranch (Dasyatis sabina). J Exp Biol 203: 2957-2966.
128. +-ATPase. J Exp Biol 204: 3251-3259.
129. Piermarini PM, Verlander JW, Royaux IE, Evans DH (2002) Pendrin immunoreactivity in the gill epithelium of a euryhaline elasmobranch. Am J Physiol 283: R983-R992.
130. Pillans RD, Franklin CE (2004) Plasma osmolyte concentrations and rectal gland mass of bull sharks Carcharhinus leucas, captured along a salinity gradient. Comp Biochem Physiol 138A: 363-371.
131. +-ATPase activity in gill, rectal gland, kidney and intestine. J Comp Physiol 175B: 37-44.
132. Pillans RD, Anderson WG, Good JP, Hyodo S, Takei Y, Hazon N, Franklin CE (2006) Plasma and erythrocyte solute properties of juvenile bull sharks, Carcharhinus leucas, acutely exposed to increasing environmental salinity. J Exp Mar Biol Ecol 331: 145-157.
133. Pillans RD, Good JP, Anderson WG, Hazon N, Franklin CE (2008) Rectal gland morphology of freshwater and seawater acclimated bull sharks Carcharhinus leucas. J Fish Biology 72: 1559-1571.
134. Quigley JP (1928) Reactions of an elasmobranch (Squalus sucklii) to variations in the salinity of the surrounding medium. Biol Bull 54: 165-190.
135. Rao GMM (1971) Influence of activity and salinity on the weight-dependent oxygen consumption of the rainbow trout Salmo gairdneri. Mar Biol 8: 205-212.
136. Raschi W, Mackanos LA (1989) The structure of the ampullae of Lorenzini in Dasyatis garouaensis and its implications on the evolution of freshwater electroreceptive systems. J Exp Zool Suppl 2: 101-111.
137. Raschi W, Keithan ED, Rhee WCH (1997) Anatomy of the ampullary electroreceptor in the freshwater stingray, Himantura signifer. Copeia 1997: 101-107.
138. Richards JG, Heigenhauser GJF, Wood CM (2003) Exercise and recovery metabolism in the Pacific spiny dogfish Squalus acanthias. J Comp Physiol 173B: 463-474.
139. Rodela TM, Ballantyne JS, Wright PA (2008) Carrier-mediated urea transport across the mitochondrial membrane of an elasmobranch (Raja erinacea) and a teleost (Oncorhynchus mykiss) fish. Am J Physiol 294: R1947-R1957.
140. Sarraseca A, Milne E, Metcalf MJ, Lobley GE (1998) Urea recycling in sheep: effects of intake. Br J Nutr 79: 79-88.
141. Scholnick DA, Mangum CP (1991) Sensitivity of hemoglobins to intracellular effectors: primitive and derived features. J Exp Zool 259: 32-42.
142. Schwarzbaum PJ, Wieser W, Niederstatter H (1991) Contrasting effects of temperature acclimation on mechanisms of ionic regulation in a eurythermic and a stenothermic species of freshwater fish (Rutilus rutilus and Salvelinus alpinus). Comp Biochem Physiol 98A: 483-489.
143. + pump to temperature change in the kidney of two species of freshwater fish, roach (Rutilus rutilus) and Arctic char (Salvelinus alpinus). Physiol Zool 65: 17-34.
144. Sezaki K, Begum RA, Wongrat P, Srivastava MP, SriKantha S, Kikuchi K, Ishihara H, Tanaka S, Taniuchi T, Watabe S (1999) Molecular phylogeny of Asian freshwater and marine stingrays based on the DNA nucleotide and deduced amino acid sequences of the cytochrome b gene. Fish Sci 65: 563-570.
145. Shuttleworth TJ (1988) Salt and water balance-extrarenal mechanisms. In: Shuttleworth TJ (ed) Physiology of elasmobranch fishes. Springer, Berlin, pp 171-199.
146. Singer TD, Ballantyne JS (1989) Absence of extrahepatic lipid oxidation in a freshwater elasmobranch, the dwarf stingray Potamotrygon magdalenae: evidence from enzyme activities. J Exp Zool 251: 355-360.
147. Singh LR, Dar TA, Ahmad F (2009) Living with urea stress. J Biosci 34: 321-331.
148. Smith HW (1931) The absorption and excretion of water and salts by the elasmobranch fishes. I. Freshwater elasmobranchs. Am J Physiol 98: 279-295.
149. Snelson FF, Williams-Hooper SE, Schmid TH (1988) Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia 1988: 729-739.
150. Speers-Roesch B (2009) The unusual energy metabolism of elasmobranchs. Comp Biochem Physiol 153A: S66.
151. Speers-Roesch B, Ip YK, Ballantyne JS (2006) Metabolic organization of freshwater, euryhaline, and marine elasmobranchs: implications for the evolution of energy metabolism in sharks and rays. J Exp Biol 209: 2495-2508.
152. Speers-Roesch B, Ip YK, Ballantyne JS (2008) Plasma non-esterified fatty acids of elasmobranchs: comparisons of temperate and tropical species and effects of environmental salinity. Comp Biochem Physiol 149A: 209-216.
153. Staurnes M, Rainuzzo JR, Sigholt T, Jorgensen L (1994) Acclimation of Atlantic cod (Gadus morhua) to cold water: stress response, osmoregulation, gill lipid composition and gill Na-K-ATPase activity. Comp Biochem Physiol 109A: 413-421.
154. Stolte H, Galaske RG, Eisenbach GM, Lechene C, Schmidt-Nielsen B, Boylan JW (1977) Renal tubule ion transport and collecting duct function in the elasmobranch little skate, Raja erinacea. J Exp Zool 199: 403-410.
155. Sulikowski JA, Maginniss LA (2001) Effects of environmental dilution on body fluid regulation in the yellow stingray, Urolophus jamaicensis. Comp Biochem Physiol 128A: 223-232.
156. Szabo T, Kalmijn AJ, Enger PS, Bullock TH (1972) Microampullary organs and a submandibular sense organ in the freshwater ray, Potamotrygon. J Comp Physiol 79: 15-27.
157. Szamier RB, Bennett MVL (1980) Ampullary electroreceptors in the freshwater ray, Potamotrygon. J Comp Physiol 138A: 225-230.
158. Tam WL, Wong WP, Loong AM, Hiong KC, Chew SF, Ballantyne JS, Ip YK (2003) The osmotic response of the Asian freshwater stingray (Himantura signifer) to increased salinity: a comparison with marine (Taeniura lymma) and Amazonian freshwater (Potamotrygon motoro) stingrays. J Exp Biol 206: 2931-2940.
159. Taniuchi T (1991) Occurrence of two species of stingrays of the genus Dasyatis (Chondrichthyes) in the Sanaga Basin, Cameroun. Environ Biol Fishes 31: 95-100.
160. Thiele I, Warth R, Bleich M, Waldegger S, Lang F, Greger R (1998) Osmotically induced conductance and capacitance changes in invitro perfused rectal gland tubules of Squalus acanthias. Kidney Blood Press Res 21: 317-324.
161. Thomerson JE, Thorson TB, Hempel RL (1977) The bull shark, Carcharhinus leucas, from the upper Mississippi River near Alton, Illinois. Copeia 1977: 166-167.
162. Thorburn DC (2006) Biology, ecology and trophic interactions of elasmobranchs and other fishes in riverine waters of Northern Australia. Thesis/Dissertation, Murdoch University.
163. Thorson TB (1962a) Body water partitioning of the freshwater shark, Carcharodon nicaraguensis compared with that of marine selachians. Am Zool 2: 452-453 (Abs#113).
164. Thorson TB (1962b) Partitioning of body fluids in the Lake Nicaragua shark and three marine sharks. Science 138: 688-690.
165. Thorson TB (1967) Osmoregulation in fresh-water elasmobranchs. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates and rays. The Johns Hopkins University Press, Baltimore, pp 265-270.
166. Thorson TB (1970) Freshwater stingrays, Potamotrygon spp.: failure to concentrate urea when exposed to saline medium. Life Sci 9: 893-900.
167. Thorson TB (1971) Movement of bull sharks, Carcharhinus leucas, between Caribbean Sea and Lake Nicaragua demonstrated by tagging. Copeia 1971: 336-338.
168. Thorson TB, Brooks DR (1983) The evolution of freshwater adaptation in stingrays. Nat Geog Soc Res Rep 15: 663-694.
169. Thorson TB, Watson DE (1975) Reassignment of the African freshwater stingray, Potamotrygon garouaensis, to the genus Dasyatis, on physiologic and morphologic grounds. Copeia 1975: 701-712.
170. Thorson TB, Watson DE, Cowan CM (1966) The status of the freshwater shark of Lake Nicaragua. Copeia 1966: 385-402.
171. Thorson TB, Cowan CM, Watson DE (1967) Potamotrygon spp.: elasmobranchs with low urea content. Science 158: 375-377.
172. Thorson TB, Cowan CM, Watson DE (1973) Body fluid solutes of juveniles and adults of the euryhaline bull shark Carcharinus leucas from freshwater and saline environments. Physiol Zool 46: 29-42.
173. Thorson TB, Wotton RM, Georgi TA (1978) Rectal gland of freshwater stingrays, Potamotrygon spp. (Chondrichthyes: Potamotrygonidae). Biol Bull 154: 508-516.
174. Thorson TB, Langhammer JK, Oetinger MI (1983) Reproduction and development of the South American freshwater stingrays, Potamotrygon circularis and P. motoro. Env Biol Fishes 9: 3-24.
175. Treberg JR, Speers-Roesch B, Piermarini PM, Ip YK, Ballantyne JS, Driedzic WR (2006) The accumulation of methylamine counteracting solutes in elasmobranchs with differing levels of urea: a comparison of marine and freshwater species. J Exp Biol 209: 860-870.
176. Urist MR (1962) Calcium and other ions in blood and skeleton of Nicaraquan fresh-water shark. Science 137: 984-986.
177. Wallman HL, Bennett WA (2006) Effects of parturition and feeding on thermal preference of Atlantic stingray Dasyatis sabina (Lesueur). Env Biol Fishes 75: 259-267.
178. Walsh PJ, Smith CP (2001) Urea transport. In: Wright PA, Anderson PM (eds) Fish physiology. Nitrogen Excretion, vol 20. Academic Press, San Diego, pp 279-307.
179. Webb JT, Brown GW (1980) Glutamine synthetase: assimilatory role in liver as related to urea retention in marine chondrichthyes. Science 208: 293-295.
180. Weber RE (1983) TMAO (Trimethylamine oxide)-independence of oxygen affinity and its urea and ATP sensitivities in an elasmobranch hemoglobin. J Exp Zool 228: 551-554.
181. Wells RMG, Weber RE (1983) Oxygenation properties and phosphorylated metabolic intermediates in blood and erythrocytes of the dogfish, Squalus acanthias. J Exp Biol 103: 95-108.
182. Wells A, Anderson WG, Hazon N (2002) Development of an in situ perfused kidney preparation for elasmobranch fish: action of arginine vasotocin. Am J Physiol 282: R1636-R1642.
183. Wells A, Anderson WG, Cains JE, Cooper MW, Hazon N (2006) Effects of angiotensin II and C-type natriuretic peptide on the in situ perfused trunk preparation of the dogfish Scyliorhinus canicula. Gen Comp Endocrinol 145: 109-115.
184. Whitehead DL (2002) Ampullary organs and electroreception in freshwater Carcharhinus leucas. J Physiol (Paris) 96: 391-395.
185. Withers PC (1998) Urea: diverse functions of a "waste" product. Clin Exp Pharmacol Physiol 25: 722-727.
186. Wong TM, 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: 85-96.
187. Wood CM (2001) Influence of feeding, exercise, and temperature on nitrogen metabolism and excretion. In: Wright PA, Anderson PM (eds) Fish physiology. Nitrogen excretion, vol. 20. Academic Press, San Diego, pp 201-238.
188. Wood CM, Part P, 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: 1545-1558.
189. Wood CM, Matsuo AYO, Gonzalez RJ, Wilson RW, Patrick ML, Val AL (2002) Mechanisms of ion transport in Potamotrygon, a stenohaline freshwater elasmobranch native to the ion-poor blackwaters of the Rio Negro. J Exp Biol 205: 3039-3054.
190. Wood CM, Matsuo AYO, Wilson RW, Gonzales RJ, Patrick ML, Playle RC, Val AL (2003) Protection by natural blackwater against disturbances in ion fluxes caused by low pH exposure in freshwater stingrays endemic to the Rio Negro. Physiol Biochem Zool 76: 12-27.
191. Wood CM, Kajimura M, Mommsen TP, Walsh PJ (2005) Alkaline tide and nitrogen conservation after feeding in an elasmobranch (Squalus acanthias). J Exp Biol 208: 2693-2705.
192. Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Am Zool 17: 379-410.
193. Wourms JP, Demski LS (1993) The reproduction and development of sharks, skates, rays and ratfishes: introduction, history, overview, and future prospects. Environ Biol Fishes 38: 7-21.
194. Wright DE (1973) The structure of the gills of the elasmobranch, Scyliorhinus canicula L. Z Zellforsch 144: 489-509.
195. Yancey PH (1994) Compatible and counteracting solutes. In: Strange K (ed) Cellular and molecular physiology of cell volume regulation. CRC Press, Boca Raton, pp 81-109.
196. Yancey PH, Somero GN (1978) Urea-requiring lactate dehydrogenases of marine elasmobranch fishes. J Comp Physiol 125B: 135-141.
197. Yancey PH, Somero GN (1979) Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes. Biochem J 183: 317-323.
198. Zammit VA, Newsholme EA (1979) Activities of enzymes of fat and ketone body metabolism and effects of starvation on blood concentrations of glucose and fat fuels in teleost and elasmobranch fish. Biochem J 184: 313-322.
199. Zeidel JD, Mathai JC, Campbell JD, Ruiz WG, Apodaca GL, Riordan J, Zeidel ML (2005) Selective permeability barrier to urea in shark rectal gland. Am J Physiol 289: F83-F89.