Fish Physiology and Biochemistry

, Volume 14, Issue 2, pp 111–123 | Cite as

Ammonia and urea excretion in the tidepool sculpin (Oligocottus maculosus): sites of excretion, effects of reduced salinity and mechanisms of urea transport

  • P. A. Wright
  • P. Part
  • C. M. Wood
Article

Abstract

Tidepool sculpins live in a variable environment where water temperature, salinity, gas tensions, and pH can change considerably with the daily tide cycle. Tidepool sculpins are primarily ammoniotelic, with 8–17% of nitrogen wastes excreted as urea. The majority of net ammonia (Jnetamm; 85%) and urea (Jneturea; 74%) excretion occurred across the gill, with the remainder excreted across the skin, the kidney, and/or gut. Acute (2h) exposure to 50% seawater significantly increased Jneturea (2.8-fold), but reduced Jnetamm (3.5-fold). In fish exposed to 50% seawater for 1 week, Jneturea returned to control values, but Jnetamm remained slightly depressed. Unidirectional urea influx (Jinurea) and efflux (Jouturea) were measured using14C-urea to determine if urea was excreted across the gills by simple diffusion or by a carrier-mediated mechanism. Jinurea increased in a linear manner with increasing urea water levels (0–11 mmol N l−1), while Jouturea was independent of external urea concentrations. As well, Jneturea and Jout inurea were not significantly different from one another, indicating the absence of “back transport”. Urea analogs and transport inhibitors added to the water did not have any consistent effect on unidirectional urea flux. These results demonstrate that ammonia and urea excretion rates and sites of excretion in tidepool sculpins are very similar to those found in other marine and freshwater teleosts. Urea and ammonia may play a role in osmoregulation as excretion rates and tissue levels were influenced by changes in water salinity. Finally, we found no evidence for a specific urea carrier; branchial urea excretion is likely dependent on simple diffusion.

Keywords

nitrogenous waste products gills unidirectional urea flux marine teleost osmoregulation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References cited

  1. Brahm, J. 1983. Urea permeability of human red cells. J. Gen. Physiol. 82: 1–23.Google Scholar
  2. Bridges, C.R. 1988. Respiratory adaptations in intertidal fish. Am. Zool. 28: 79–96.Google Scholar
  3. Boylan, J. 1967. Gill Permeability inSqualus acanthias.In Sharks, Skates and Rays. pp. 197–206. Edited by P.W. Gilbert, R.F. Mathewson and D.P. Rall, John Hopkins Press, Baltimore.Google Scholar
  4. Cameron, J.N. and Heisler, N. 1983. Studies of ammonia in the rainbow trout: physico-chemical parameters, acid-base behaviour, and respiratory clearance. J. Exp. Biol. 105: 107–125.Google Scholar
  5. Chou, C.L. and Knepper, M.A. 1989. Inhibition of urea transport in inner medullary collecting duct by phloretin and urea analogues. Am. J. Physiol. 257: F359–F365.Google Scholar
  6. Claiborne, J.B. and Perry, E. 1991. Acid-base transfers in the long-horn sculpin (Myoxocephalus octodecimspinosus) following exposure to 20% seawater and low external chloride. Bull. Mt. Desert Island Biol. Lab. 30: 107–108.Google Scholar
  7. Curci, S., Casavola, V., Cremaschi, D. and Lippe, C. 1976. Facilitated transport of urea across the toad gallbladder. Pflugers Arch. 362: 109–112.Google Scholar
  8. Daikoku, T., Yano, I. and Masui, M. 1982. Lipid and fatty acid compositions and their changes in the different organs and tissues of guppy,Poecilia reticulata on sea water adaptation. Comp. Biochem. Physiol. 73A: 167–174.Google Scholar
  9. Davenport, J. and Sayer, M.D.J. 1986. Ammonia and urea excretion in the amphibious teleostBlennius pholis (L.) in seawater and in air. Comp. Biochem. Physiol. 84A: 189–194.Google Scholar
  10. Dejours, P. 1981. Principles of Comparative Respiratory Physiology, 2nd edition. Elsevier/North Holland, Amsterdam.Google Scholar
  11. Effros, R.M., Murphy, C., Hacker, A. and Ozker, K. 1992. Presence of urea transporters in the liver but not the lungs. FASEB J. 6: A2073.Google Scholar
  12. Evans, D.H., More, K.J. and Robbins, S.L. 1989. Modes of ammonia transport across the gill epithelium of the marine teleost fish,Opsanus beta. J. Exp. Biol. 144: 339–356.Google Scholar
  13. Evans, D.H. 1993. Osmotic and ionic regulation.In The Physiology of Fishes. pp. 315–341. Edited by D.H. Evans. CRC Press, Baton Rouge.Google Scholar
  14. Evans, D.H. and Cameron, J.N. 1986. Gill ammonia transport. J. Exp. Zool. 239: 17–23.Google Scholar
  15. Forster, R.P. and Goldstein, L. 1976. Intracellular osmoregulatory role of amino acids and urea in marine elasmobranchs. Am. J. Physiol. 230: 925–931.Google Scholar
  16. Goldstein, L., Oppcit, W.W. and Maren, T.H. 1968. Osmotic regulation and urea metabolism in the lemon shark,Negaprion brevirostris. Am. J. Physiol. 215: 1493–1497.Google Scholar
  17. Goldstein, L. and Forster, R.P. 1971. Osmoregulation and urea metabolism in the little skate,Raja crinacea. Am. J. Physiol. 222: 742–746.Google Scholar
  18. Gordon, M.S., Boetius, I., Evans, D.H., McCarthy, R. and Oglesby, L.C. 1965. Salinity adaptation in the mudskipper fish,Periophthalmus sabrinus. Hvalradets Skrifter Norske Videnskap Akad., Oslo. 48: 85–93.Google Scholar
  19. Hays, R.M., Levine, S.D., Myers, J.D., Heinemann, H.O., Kaplan, M.A., Franki, N. and Berliner, H. 1977. Urea transport in the dogfish kidney. J. Exp. Zool. 199: 309–316.Google Scholar
  20. Horn, M.H. and Gibson, R.N. 1988. Intertidal fishes. Sci. Am. January: 64–70.Google Scholar
  21. Isaia, J., Girard, J.P. and Payan, P. 1978. Kinetic study of gill epithelium permeability of water diffusion in the fresh water trout,Salmo gairdneri: effect of adrenaline. J. Membrane Biol. 41: 337–347.Google Scholar
  22. Isaia, J. 1982. Effects of environmental salinity on branchial permeability of rainbow trout,Salmo gairdneri. J. Physiol. 326: 297–307.Google Scholar
  23. Kaplan, M.A., Hays, L. and Hays, R.M. 1974. Evolution of a facilitated diffusion pathway for amides in the erythrocyte. Am. J. Physiol. 226: 1327–1332.Google Scholar
  24. Katz, U., Garcia-Romeu, F., Masoni, A. and Isaia, J. 1981. Active transport of urea across the skin of the euryhaline toad,Bufo viridis. Pflugers Archiv. 390: 299–300.Google Scholar
  25. Kormanik, G.A. and Evans, D.H. 1991. Nitrogenous waste excretion in the intertidal rock gunnel: the effects of emersion. Bull. Mt. Desert Is. Bio. Lab. pp. 33–35.Google Scholar
  26. Lacoste, I, Dunel-Erb, S., Harvey, B.J, Laurent, P. and Ehrenfeld, J. 1991. Active urea transport independent of H+ and Na+ transport in frog skin epithelium. Am. J. Physiol. 261: R898–R906.Google Scholar
  27. Laming, P.R., Funston, C.W., Roberts, D. and Armstrong, M.J. 1982. Behavioural, physiological and morphological adaptations of the shanny (Blennius pholis) to the intertidal habitat. J. Mar. Biol. Ass. U.K. 62: 329–338.Google Scholar
  28. Levine, S., Franki, N. and Hays, R.M. 1973. Effect of phloretin on water and solute movement in the toad bladder. Clin. Invest. 52: 1435–1442.Google Scholar
  29. Maetz, J. 1972. Branchial sodium exchange and ammonia excretion in the goldfish,Carassius auratus. Effects of ammonia loading and temperature changes. J. Exp. Biol. 56: 601–620.Google Scholar
  30. Harsh, D.J. and Knepper, M.A. 1992. Renal handling of urea.In Handbook of Physiology. Section 8. Renal Physiology. Edited by E.E. Windhager. Oxford University Press, New York.Google Scholar
  31. Martial, S., Neau, P., Degeilh, F., Lamotte, H., Rousseau, B. and Ripoche, P. 1993. Urea derivatives as tools for studying the urea-facilitated transport system. Pflugers Arch. 423: 51–58.Google Scholar
  32. Masoni, A. and Payan, P. 1974. Urea, insulin and para-amino-hippuric acid (PAH) excretion by the gills of the eel,Anguilla anguilla L. Comp. Biochem. Physiol. 47A: 1241–1244.Google Scholar
  33. Mayrand, R.R. and Levitt, D.G. 1983. Urea and ethylene glycol-facilitated transport systems in the human red cell membrane. J. Gen. Physiol. 81: 221–237.Google Scholar
  34. Mommsen, T.P. and Walsh, P.J. 1989. Evolution of urea synthesis in vertebrates: the piscine connection. Science 243: 72–75.Google Scholar
  35. Morii, H., Nishikata, K. and Tamura, O. 1978. Nitrogen excretion of mudskipper fishPeriophthalmus cantonensis andBoleophthalmus pectinorostris in water and on land. Comp. Biochem. Physiol. 60A: 189–193.Google Scholar
  36. Payan, P., Goldstein, L. and Forster, R.P. 1973. Gills and kidneys in ureosmotic regulation in euryhaline skates. Am. J. Physiol. 224: 367–372.Google Scholar
  37. Pelster, B., Bridges, C.R. and Grieshaber, M.K. 1988. Physiological adaptations of the intertidal rockpool teleost,Blennius pholis L., to aerial exposure. Resp Physiol. 71: 355–374.Google Scholar
  38. Potts, W.T.W. 1984. Transepithelia potentials in fish gills.In Fish Physiology. Vol 10B, pp. 326–388. Edited by U.S. Hoar and D.J. Randall. Academic Press, New York.Google Scholar
  39. Rahmatullah, M. and Boyde, T.R.C. 1980. Improvements in the determination of urea using diacetyl monoxime; methods with and without deproteinisation. Clin. Chim. Acta. 107: 3–9.Google Scholar
  40. Rapoport, J., Chaimivitz, C. and Hays, R.M. 1989. Active urea transport in toad skin is coupled to H+ gradients. Am. J. Physiol. 256: F830–F835.Google Scholar
  41. Read, L.J. 1968. A study of ammonia and urea production and excretion in the freshwater-adapted form of the Pacific lamprey,Entosphenus tridentatus. Comp. Biochem. Physiol. 26: 455–466.Google Scholar
  42. Rozemeijer, M.J.C. and Plaut, I. 1993. Regulation of nitrogen excretion of the amphibious BlenniidaeAlticus kirki (Guenther, 1868) during emersion and immersion. Comp. Biochem. Physiol. 10A: 57–62.Google Scholar
  43. Sayer, M.D.J. and Davenport, J. 1987a. Ammonia and urea excretion in the amphibious teleostBlennius pholis exposed to fluctuating salinity and pH. Comp. Biochem. Physiol. 87A: 851–857.Google Scholar
  44. Sayer, M.D.J. and Davenport, J. 1987b. The relative importance of the gills to ammonia and urea excretion in five seawater and one freshwater teleost species. J. Fish. Biol. 31: 561–570.Google Scholar
  45. Schmidt-Nielsen, B. and Rabinowitz, L. 1964. Methylurea and acetamide: active reabsorption by elasmobranch renal tubules. Science 146: 1587–1588.Google Scholar
  46. Smith, H.W. 1929. The excretion of ammonia and urea by the gills of fish. J. Biol. Chem. 81: 727–742.Google Scholar
  47. Verdouw, H., Van Echted, C.J.A. and Dekkers, E.M.J. 1978. Ammonia determination based on indophenol formation with sodium salicylate. Water Res. 12: 399–402.Google Scholar
  48. Walsh, P.J., Tucker, B.C. and Hopkins, T.E. 1994. Effects of confinement/crowding on ureogenesis in the gulf toadfish,Opsanus beta. J. Exp. Biol. 191: 195–206.Google Scholar
  49. Wood, C.M. 1993. Ammonia and urea metabolism and excretion.In The Physiology of Fishes. pp. 379–425. Edited by D.H. Evans. CRC Press, Baton Rouge.Google Scholar
  50. Wright, P.A. 1993. Nitrogen excretion and enzyme pathways for ureagenesis in freshwater tilapia (Oreochromis niloticus). Physiol. Zool. 66: 881–901.Google Scholar
  51. Wright, P.A. and Wood, C.M. 1985. An analysis of branchial ammonia excretion in the freshwater rainbow trout: effects of environment pH change and sodium uptake blockade. J. Exp. Biol. 114: 329–353.Google Scholar
  52. Wright, P.A., Iwama, G.K. and Wood, C.H. 1993. Ammonia and urea excretion in Lahontan cutthroat troutOncorhynchus clarki henshawi adapted to the highly alkaline Pyramid Lake. J. Exp. Biol. 175: 153–172.Google Scholar
  53. Zwingelstein, G. 1979–1980. Les effets de l'adaptation à l'eau de mer sur le métabolism lipidique du poisson. Oceanis 5: 117–130.Google Scholar

Copyright information

© Kugler Publications 1995

Authors and Affiliations

  • P. A. Wright
    • 1
  • P. Part
    • 2
  • C. M. Wood
    • 3
  1. 1.Department of ZoologyUniversity of GuelphGuelphCanada
  2. 2.Department of EcotoxicologyUppsala UniversityUppsalaSweden
  3. 3.Department of BiologyMcMaster UniversityHamiltonCanada

Personalised recommendations