Journal of Comparative Physiology B

, Volume 180, Issue 4, pp 475–493 | Cite as

Freshwater elasmobranchs: a review of their physiology and biochemistry

  • James S. BallantyneEmail author
  • J. W. Robinson


Only 5% of elasmobranch species live in freshwater (FW) compared to more than 40% of known teleost species. The factors affecting the poor penetration of elasmobranchs into FW environments are currently unknown, however, an important consideration may be the high urea requirement of many proteins in marine elasmobranchs. Urea is an important osmolyte in marine elasmobranchs and must be reduced in dilute environments. There are three identifiable stages in the successful colonization of FW. The euryhaline marine species freely entering and leaving FW represent the initial stage of FW colonization. In this group, there is an apparent inability to eliminate all urea due to protein integrity issues and this results in energy and nitrogen losses that may constrain growth and reproduction. The second stage is represented by those species that live entirely in FW but must also retain some urea. This group also suffers from the same constraints as the first group. These two groups have kidneys and sensory organs that more closely resemble strictly marine forms. The third and final stage is represented by the Potamotrygonid stingrays where the need for urea in FW has been eliminated. Consequently nitrogen and energy losses are reduced and those sections of the kidney needed for urea conservation have been eliminated. The driving force for such modifications is a reduction in urea levels and the concomitant saving of energy needed for urea synthesis. Other physiological adaptations associated with survival in FW include giving birth to live young, the capacity of sperm to be activated in freshwater and modifications of the electrosensory system to function in a low conductivity environment. The need for many anatomical, metabolic and physiological modifications for FW existence may constrain the rapidity and hence the frequency of FW colonization, compared to the situation in the more advanced osmoregulating teleosts. Once optimally adapted to FW, recolonization of sea water by elasmobranchs is problematic due to the loss of urea synthetic capacity and renal structures for urea retention.


Elasmobranch Freshwater Metabolism Osmoregulation Salinity Physiology 


  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 284:475–484PubMedGoogle Scholar
  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 144:90–98Google Scholar
  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 147:39–46PubMedGoogle Scholar
  4. Anderson WG, Taylor JR, Good JP, Hazon N, Grosell M (2007) Body fluid volume regulation in elasmobranch fish. Comp Biochem Physiol 148A:3–13Google Scholar
  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:S65Google Scholar
  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 138:275–282PubMedGoogle Scholar
  7. Ballantyne JS (1997) Jaws, the inside story. The metabolism of elasmobranch fishes. Comp Biochem Physiol 118B:703–742Google Scholar
  8. Ballantyne JS, Moon TW (1986) Solute effects on mitochondria from an elasmobranch (Raja erinacea) and teleost (Pseudopleuronectes americanus). J Exp Zool 239:319–328PubMedGoogle Scholar
  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 238:267–271Google Scholar
  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–R808PubMedGoogle Scholar
  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 75:2129–2136Google Scholar
  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:9–13Google Scholar
  13. Bonaventura J, Bonaventura C, Sullivan B (1974) Urea tolerance as a molecular adaptation of elasmobranch hemoglobins. Science 186:57–59PubMedGoogle Scholar
  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 197–206Google Scholar
  15. Boylan JW, Feldman B, Antowiak D (1963) Factors affecting gill permeability in Squalus acanthias. Bull Mount Desert Island Biol Lab 5:29Google Scholar
  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 147–175Google Scholar
  17. Cain DK, Harms CA, Segars A (2004) Plasma biochemistry reference values of wild-caught southern stingrays (Dasyatis americana). J Zoo Wildl Med 35:471–476PubMedGoogle Scholar
  18. Cameron JN (1986) Responses to reversed NH3 and NH4 + gradients in a teleost (Ictalurus punctatus), an elasmobranch (Raja erinacea), and a crustacean (Callinectes sapidus): evidence for NH4 +/H+ exchange in the teleost and the elasmobranch. J Exp Zool 239:183–195PubMedGoogle Scholar
  19. Carrier JC, Evans DH (1972) Ion, water and urea turnover rates in the nurse shark, Ginglymostoma cirratum. Comp Biochem Physiol 41A:761–764Google Scholar
  20. Carrier JC, Evans DH (1973) Ion and water turnover in the fresh-water elasmobranch Potamotrygon sp. Comp Biochem Physiol 45A:667–670Google Scholar
  21. Chamberlin ME, Ballantyne JS (1992) Glutamine metabolism in elasmobranch and agnathan muscle. J Exp Zool 264:269–272Google Scholar
  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 35:165–171Google Scholar
  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 52:123–131Google Scholar
  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 209:484–492PubMedGoogle Scholar
  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:52–63Google Scholar
  26. Choe KP, Verlander JW, Wingo CS, Evans DH (2004) A putative H+-K+-ATPase in the Atlantic stingray, Dasyatis sabina: primary sequence and expression in the gills. Am J Physiol 287:R981–R991Google Scholar
  27. Choe KP, Edwards SL, Claiborne JB, Evans DH (2007) The putative mechanism of Na+ absorption in euryhaline elasmobranchs exists in the gills of a stenohaline marine elasmobranch, Squalus acanthias. Comp Biochem Physiol 146A:155–162Google Scholar
  28. Coelho R, Erzini K (2006) Reproductive aspects of the undulate ray, Raja undulata, from the south coast of Portugal. Fish Res 81:80–85Google Scholar
  29. Cohen DM (1970) How many recent fishes are there? Proc Calif Acad Sci 38:341–346Google Scholar
  30. Cohen JJ, Krupp MA, Chidsey CA (1958) Renal conservation of trimethylamine oxide by the spiny dogfish, Squalus acanthias. Am J Physiol 194:229–235PubMedGoogle Scholar
  31. Compagno LJV (1995) The exploitation and conservation of freshwater elasmobranchs: status of taxa and prospects for the future. J Aquaric Aquat Sci 7:62–90Google Scholar
  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:211–222Google Scholar
  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 132:29–42Google Scholar
  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:895–903Google Scholar
  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:223–236Google Scholar
  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–S66Google Scholar
  37. De Almeida-Val VMF, Val AL (1993) Evolutionary trends of LDH isozymes in fishes. Comp Biochem Physiol 105B:21–28Google Scholar
  38. de Vlaming VL, Sage M (1973) Osmoregulation in the euryhaline elasmobranch, Dasyatis sabina. Comp Biochem Physiol 45A:31–44Google Scholar
  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:118–127Google Scholar
  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 213:210–224PubMedGoogle Scholar
  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 274:327–333Google Scholar
  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 106:25–41PubMedGoogle Scholar
  43. Evans DH (1969) Studies on the permeability to water of selected marine, freshwater and euryhaline teleosts. J Exp Biol 50:689–703PubMedGoogle Scholar
  44. Evans DH (1981) The egg case of the oviparous elasmobranch Raja erinacea, does osmoregulate. J Exp Biol 92:337–340Google Scholar
  45. Evans DH (1984) Gill Na+/H+ and Cl/HCO3- exchange systems evolved before the vertebrates entered freshwater. J Exp Biol 113:465–469PubMedGoogle Scholar
  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 247–268Google Scholar
  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 85:97–177PubMedGoogle Scholar
  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–R24Google Scholar
  49. Forster RP, Goldstein L (1976) Intracellular osmoregulatory role of amino acids and urea in marine elasmobranchs. Am J Physiol 230:925–931PubMedGoogle Scholar
  50. Forster RP, Hannafin JA, Goldstein L (1978) Osmoregulatory role of amino acids in brain of the elasmobranch, Raja erinacea. Comp Biochem Physiol 60A:25–30Google Scholar
  51. Foulley M, Mellinger J (1980) La diffusion de l’eau tritiees, de l’uree 14C et d’autres substances a travers la coque de l’ouef de Rousette, Scyliorhinus canicula. C R Acad Sci Paris 290:427–430Google Scholar
  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 287–323Google Scholar
  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:87–93Google Scholar
  54. Goldstein L, Brill SR (1991) Volume-activated taurine efflux from skate erythrocytes: possible band 3 involvement. Am J Physiol 260:R1014–R1020PubMedGoogle Scholar
  55. Goldstein L, Forster RP (1970) Urea biosynthesis and excretion in freshwater and marine elasmobranchs. Bull Mount Desert Island Biol Lab 10:20–22Google Scholar
  56. Goldstein L, Forster RP (1971a) Osmoregulation and urea metabolism in the little skate Raja erinacea. Am J Physiol 220:742–746PubMedGoogle Scholar
  57. Goldstein L, Forster RP (1971b) Urea biosynthesis and excretion in freshwater and marine elasmobranchs. Comp Biochem Physiol 39B:415–421Google Scholar
  58. Goldstein L, Oppelt WW, Maren TH (1968) Osmotic regulation and urea metabolism in the lemon shark Negaprion brevirostris. Am J Physiol 215:1493–1497PubMedGoogle Scholar
  59. Goldstein L, Claiborne JB, Evans DE (1982) Ammonia excretion by the gills of two marine teleost fish: the importance of NH4 + permeance. J Exp Zool 219:395–397PubMedGoogle Scholar
  60. Griffith RW, Pang PKT, Srivastava K, Pickford GE (1973) Serum composition of freshwater stringrays (Potamotrygonidae) adapted to freshwater and dilute seawater. Biol Bull 144:304–320Google Scholar
  61. Hamlett WC (1999) Male reproductive system. In: Hamlett WC (ed) Sharks, skates and rays. The Johns Hopkins University Press, Baltimore, pp 444–447Google Scholar
  62. Hammerschlag N (2006) Osmoregulation in elasmobranchs: a review for fish biologists, behaviourists and ecologists. Mar Freshw Behav Physiol 39:209–228Google Scholar
  63. Haynes JK, Goldstein L (1993) Volume-regulatory amino acid transport in erythrocytes of the little skate, Raja erinacea. Am J Physiol 265:R173–R179PubMedGoogle Scholar
  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 26:69–75Google Scholar
  65. Hazon N, Henderson IW (1984) Secretory dynamics of 1alpha-hydroxycorticosterone in the elasmobranch fish, Scyliorhinus canicula. J Endocrinol 103:205–211PubMedGoogle Scholar
  66. Hazon N, Tiersch TR, Takei Y (1999) Renin–angiotensin system in elasmobranch fish: a review. J Exp Zool 284:526–534PubMedGoogle Scholar
  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:685–700Google Scholar
  68. Heffron JK, Moerland TS (2008) Parvalbumin characterization from the euryhaline stingray Dasyatis sabina. Comp Biochem Physiol 150A:339–346Google Scholar
  69. Helfman GS, Collette BB, Facey DE (1997) The diversity of fishes. Blackwell, MaldenGoogle Scholar
  70. Heupel MR, Simpfendorfer CA (2008) Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquat Biol 1:277–289Google Scholar
  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 1–89Google Scholar
  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 207:347–356PubMedGoogle Scholar
  73. Hyodo S, Tsukada T, Takei Y (2004b) Neurohypophysial hormones of dogfish, Triakis scyllium: structures and salinity-dependent secretion. Gen Comp Endocrinol 138:97–104PubMedGoogle Scholar
  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 9:457–477PubMedGoogle Scholar
  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 206:3625–3633PubMedGoogle Scholar
  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 78:610–619PubMedGoogle Scholar
  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 212:3828–3836PubMedGoogle Scholar
  78. Jampol LM, Epstein FM (1970) Sodium–potassium-activated adenosinetriphosphatase and osmotic regulation by fishes. Am J Physiol 218:607–611PubMedGoogle Scholar
  79. Janech MG, Piermarini PM (2002) Renal water and solute excretion in the Atlantic stingray in freshwater. J Fish Biology 61:1053–1057Google Scholar
  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–F1005Google Scholar
  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–R853Google Scholar
  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–F780Google Scholar
  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 539–559Google Scholar
  84. Johansen K, Mangum CP, Lykkeboe G (1978) Respiratory properties of the blood of Amazon fishes. Can J Zool 56:898–906Google Scholar
  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 59:74–88Google Scholar
  86. Kempton RT (1953) Studies on the elasmobranch kidney. II. Reabsorption of urea by the smooth dogfish, Mustelus canis. Biol Bull 104:45–56Google Scholar
  87. Kennedy PM, Hume ID (1978) Recycling of urea nitrogen to the gut of the tammar wallaby (Macropus eugenii). Comp Biochem Physiol 61A:117–121Google Scholar
  88. King PA, Goldstein L (1983a) Organic osmolytes and cell volume regulation in fish. Mol Physiol 4:53–66Google Scholar
  89. King PA, Goldstein L (1983b) Renal ammoniagenesis and acid excretion in the dogfish, Squalus acanthias. Am J Physiol 245:R581–R589PubMedGoogle Scholar
  90. Kirschner LB (1993) The energetics of osmotic regulation in ureotelic and hypoosmotic fishes. J Exp Zool 267:19–26Google Scholar
  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 107–146Google Scholar
  92. Lewiston N, Newman A, Robin E, Holtzman D (1979) Shark heart mitochondria: effects of external osmolality on respiration. Science 206:75–76PubMedGoogle Scholar
  93. Lovejoy NR, Bermingham E, Martin AP (1998) Marine incursion into South America. Nature 396:421–422Google Scholar
  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:185–200Google Scholar
  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 63:345–353Google Scholar
  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:127–131Google Scholar
  97. Mangum CP, Haswell MS, Johansen K (1977) Low salt and high pH in the blood of Amazon fishes. J Exp Zool 200:163–168Google Scholar
  98. Martin RA (2005) Conservation of freshwater and euryhaline elasmobranchs. J Mar Biol Ass UK 85:1049–1073Google Scholar
  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:131–138Google Scholar
  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 55–133Google Scholar
  101. McGowan DW, Kajiura SM (2009) Electroreception in the euryhaline stingray, Dasyatis sabina. J Exp Biol 212:1544–1552PubMedGoogle Scholar
  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:S93Google Scholar
  103. Meloni CJ, Cech JJ, Katzman SM (2002) Effect of brackish salinities on oxygen consumption of bat rays (Myliobatis californica). Copeia 2002:462–465Google Scholar
  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 206:3285–3292PubMedGoogle Scholar
  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 206:3202–3293Google Scholar
  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 51:529–546PubMedGoogle Scholar
  107. Moyes CD, Moon TW, Ballantyne JS (1986) Osmotic effects on amino acid oxidation in skate liver mitochondria. J Exp Biol 125:181–195PubMedGoogle Scholar
  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:189–193Google Scholar
  109. Musch MW, Goldstein L (1996) High affinity binding of ankyrin induced by volume expansion in skate erythrocytes. J Biol Chem 271:21221–21225PubMedGoogle Scholar
  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 279:39447–39453PubMedGoogle Scholar
  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 99:9231–9236PubMedGoogle Scholar
  112. Nunez S, Trant JM (1999) Regulation on interrenal gland steroidogenesis in the Atlantic stingray (Dasyatis sabina). J Exp Zool 284:517–525PubMedGoogle Scholar
  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 35:557–569PubMedGoogle Scholar
  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:306–317Google Scholar
  115. Ogawa M, Hirano T (1982) Studies of the nephron of a freshwater stingray, Potamotrygon magdalenae. Zool Mag 91:101–105Google Scholar
  116. Oguri M (1964) Rectal glands of marine and fresh-water sharks: comparative histology. Science 144:1151–1152PubMedGoogle Scholar
  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 329–352Google Scholar
  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 29:147–153Google Scholar
  119. Pang PKT, Griffith RW, Atz JW (1977) Osmoregulation in elasmobranchs. Am Zool 17:365–377Google Scholar
  120. Pang PKT, Furspan PB, Sawyer WH (1983) Evolution of neurohypophyseal hormone actions in vertebrates. Am Zool 23:655–662Google Scholar
  121. Part P, Wright PA, Wood CM (1998) Urea and water permeability in dogfish (Squalus acanthias) gills. Comp Biochem Physiol 119A:117–123Google Scholar
  122. Payan P, Maetz J (1971) Balance hydrique chez les elasmobranches: arguments en faveur d’un controle endocrinien. Gen Comp Endocrinol 16:535–554PubMedGoogle Scholar
  123. Payan P, Matty AJ (1975) The characteristics of ammonia excretion by a perfused isolated head of trout (Salmo gairdneri): effect of temperature and CO2-free ringer. J Comp Physiol 96:167–184Google Scholar
  124. Payan P, Goldstein L, Forster RP (1973) Gills and kidneys in ureosmotic regulation in euryhaline skates. Am J Physiol 224:367–372PubMedGoogle Scholar
  125. Perlman L, Goldstein DF (1988) Nitrogen metabolism. In: Shuttleworth TJ (ed) Physiology of elasmobranch fishes. Springer, New York, pp 253–275Google Scholar
  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 71:553–560PubMedGoogle Scholar
  127. Piermarini PM, Evans DH (2000) Effects of environmental salinity on Na+/K+-ATPase in the gills and rectal gland of a euryhaline elasmobranch (Dasyatis sabina). J Exp Biol 203:2957–2966PubMedGoogle Scholar
  128. Piermarini PM, 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 204:3251–3259PubMedGoogle Scholar
  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–R992Google Scholar
  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:363–371Google Scholar
  131. Pillans RD, Good JP, Anderson WG, Hazon N, Franklin CE (2005) Freshwater to seawater acclimation of juvenile bull sharks (Carcharhinus leucas): plasma osmolytes and Na+/K+-ATPase activity in gill, rectal gland, kidney and intestine. J Comp Physiol 175B:37–44Google Scholar
  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 331:145–157Google Scholar
  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 72:1559–1571Google Scholar
  134. Quigley JP (1928) Reactions of an elasmobranch (Squalus sucklii) to variations in the salinity of the surrounding medium. Biol Bull 54:165–190Google Scholar
  135. Rao GMM (1971) Influence of activity and salinity on the weight-dependent oxygen consumption of the rainbow trout Salmo gairdneri. Mar Biol 8:205–212Google Scholar
  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 2:101–111Google Scholar
  137. Raschi W, Keithan ED, Rhee WCH (1997) Anatomy of the ampullary electroreceptor in the freshwater stingray, Himantura signifer. Copeia 1997:101–107Google Scholar
  138. Richards JG, Heigenhauser GJF, Wood CM (2003) Exercise and recovery metabolism in the Pacific spiny dogfish Squalus acanthias. J Comp Physiol 173B:463–474Google Scholar
  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–R1957Google Scholar
  140. Sarraseca A, Milne E, Metcalf MJ, Lobley GE (1998) Urea recycling in sheep: effects of intake. Br J Nutr 79:79–88PubMedGoogle Scholar
  141. Scholnick DA, Mangum CP (1991) Sensitivity of hemoglobins to intracellular effectors: primitive and derived features. J Exp Zool 259:32–42Google Scholar
  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:483–489Google Scholar
  143. Schwarzbaum PJ, Wieser W, Cossins AR (1992) Species-specific responses of membranes and the Na+/K+ pump to temperature change in the kidney of two species of freshwater fish, roach (Rutilus rutilus) and Arctic char (Salvelinus alpinus). Physiol Zool 65:17–34Google Scholar
  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 65:563–570Google Scholar
  145. Shuttleworth TJ (1988) Salt and water balance—extrarenal mechanisms. In: Shuttleworth TJ (ed) Physiology of elasmobranch fishes. Springer, Berlin, pp 171–199Google Scholar
  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 251:355–360Google Scholar
  147. Singh LR, Dar TA, Ahmad F (2009) Living with urea stress. J Biosci 34:321–331PubMedGoogle Scholar
  148. Smith HW (1931) The absorption and excretion of water and salts by the elasmobranch fishes. I. Freshwater elasmobranchs. Am J Physiol 98:279–295Google Scholar
  149. Snelson FF, Williams-Hooper SE, Schmid TH (1988) Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia 1988:729–739Google Scholar
  150. Speers-Roesch B (2009) The unusual energy metabolism of elasmobranchs. Comp Biochem Physiol 153A:S66Google Scholar
  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 209:2495–2508PubMedGoogle Scholar
  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:209–216Google Scholar
  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:413–421Google Scholar
  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 199:403–410PubMedGoogle Scholar
  155. Sulikowski JA, Maginniss LA (2001) Effects of environmental dilution on body fluid regulation in the yellow stingray, Urolophus jamaicensis. Comp Biochem Physiol 128A:223–232Google Scholar
  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 79:15–27Google Scholar
  157. Szamier RB, Bennett MVL (1980) Ampullary electroreceptors in the freshwater ray, Potamotrygon. J Comp Physiol 138A:225–230Google Scholar
  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 206:2931–2940PubMedGoogle Scholar
  159. Taniuchi T (1991) Occurrence of two species of stingrays of the genus Dasyatis (Chondrichthyes) in the Sanaga Basin, Cameroun. Environ Biol Fishes 31:95–100Google Scholar
  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 21:317–324PubMedGoogle Scholar
  161. Thomerson JE, Thorson TB, Hempel RL (1977) The bull shark, Carcharhinus leucas, from the upper Mississippi River near Alton, Illinois. Copeia 1977:166–167Google Scholar
  162. Thorburn DC (2006) Biology, ecology and trophic interactions of elasmobranchs and other fishes in riverine waters of Northern Australia. Thesis/Dissertation, Murdoch UniversityGoogle Scholar
  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)Google Scholar
  164. Thorson TB (1962b) Partitioning of body fluids in the Lake Nicaragua shark and three marine sharks. Science 138:688–690PubMedGoogle Scholar
  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 265–270Google Scholar
  166. Thorson TB (1970) Freshwater stingrays, Potamotrygon spp.: failure to concentrate urea when exposed to saline medium. Life Sci 9:893–900Google Scholar
  167. Thorson TB (1971) Movement of bull sharks, Carcharhinus leucas, between Caribbean Sea and Lake Nicaragua demonstrated by tagging. Copeia 1971:336–338Google Scholar
  168. Thorson TB, Brooks DR (1983) The evolution of freshwater adaptation in stingrays. Nat Geog Soc Res Rep 15:663–694Google Scholar
  169. Thorson TB, Watson DE (1975) Reassignment of the African freshwater stingray, Potamotrygon garouaensis, to the genus Dasyatis, on physiologic and morphologic grounds. Copeia 1975:701–712Google Scholar
  170. Thorson TB, Watson DE, Cowan CM (1966) The status of the freshwater shark of Lake Nicaragua. Copeia 1966:385–402Google Scholar
  171. Thorson TB, Cowan CM, Watson DE (1967) Potamotrygon spp.: elasmobranchs with low urea content. Science 158:375–377PubMedGoogle Scholar
  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 46:29–42Google Scholar
  173. Thorson TB, Wotton RM, Georgi TA (1978) Rectal gland of freshwater stingrays, Potamotrygon spp. (Chondrichthyes: Potamotrygonidae). Biol Bull 154:508–516PubMedGoogle Scholar
  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 9:3–24Google Scholar
  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 209:860–870PubMedGoogle Scholar
  176. Urist MR (1962) Calcium and other ions in blood and skeleton of Nicaraquan fresh-water shark. Science 137:984–986PubMedGoogle Scholar
  177. Wallman HL, Bennett WA (2006) Effects of parturition and feeding on thermal preference of Atlantic stingray Dasyatis sabina (Lesueur). Env Biol Fishes 75:259–267Google Scholar
  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 279–307Google Scholar
  179. Webb JT, Brown GW (1980) Glutamine synthetase: assimilatory role in liver as related to urea retention in marine chondrichthyes. Science 208:293–295PubMedGoogle Scholar
  180. Weber RE (1983) TMAO (Trimethylamine oxide)-independence of oxygen affinity and its urea and ATP sensitivities in an elasmobranch hemoglobin. J Exp Zool 228:551–554PubMedGoogle Scholar
  181. Wells RMG, Weber RE (1983) Oxygenation properties and phosphorylated metabolic intermediates in blood and erythrocytes of the dogfish, Squalus acanthias. J Exp Biol 103:95–108PubMedGoogle Scholar
  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–R1642Google Scholar
  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 145:109–115PubMedGoogle Scholar
  184. Whitehead DL (2002) Ampullary organs and electroreception in freshwater Carcharhinus leucas. J Physiol (Paris) 96:391–395Google Scholar
  185. Withers PC (1998) Urea: diverse functions of a “waste” product. Clin Exp Pharmacol Physiol 25:722–727PubMedGoogle Scholar
  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 200:85–96Google Scholar
  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 201–238Google Scholar
  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 198:1545–1558PubMedGoogle Scholar
  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 205:3039–3054PubMedGoogle Scholar
  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 76:12–27PubMedGoogle Scholar
  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 208:2693–2705PubMedGoogle Scholar
  192. Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Am Zool 17:379–410Google Scholar
  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 38:7–21Google Scholar
  194. Wright DE (1973) The structure of the gills of the elasmobranch, Scyliorhinus canicula L. Z Zellforsch 144:489–509PubMedGoogle Scholar
  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 81–109Google Scholar
  196. Yancey PH, Somero GN (1978) Urea-requiring lactate dehydrogenases of marine elasmobranch fishes. J Comp Physiol 125B:135–141Google Scholar
  197. Yancey PH, Somero GN (1979) Counteraction of urea destabilization of protein structure by methylamine osmoregulatory compounds of elasmobranch fishes. Biochem J 183:317–323PubMedGoogle Scholar
  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 184:313–322PubMedGoogle Scholar
  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–F89CrossRefGoogle Scholar

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© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Integrative BiologyUniversity of GuelphGuelphCanada

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