Consequences of High Levels of Ammonia Exposure on the Gills Epithelium and on the Haematological Characteristics of the Blood of the Siberian Sturgeon, Acipenser baerii

  • Guy Nonnotte
  • Dominique Salin
  • Patrick Williot
  • Karine Pichavant-Rafini
  • Michel Rafini
  • Liliane Nonnotte


Ammonia toxicity in the Siberian sturgeon, Acipenser baerii, a fresh water fish, was studied under controlled conditions of pH, temperature and ammonia concentrations in water.The effects of ammonia during a 72-h exposure to lethal and sublethal doses were examined on the morphology of branchial epithelium. Some hypertrophies and necrosis were observed in proportion with the ammonia doses.Ammonia has no effect on haematological characteristics except for the [K+] plasmatic concentration and the erythrocyte volume for lethal levels of ammonia.Among the numerous hypotheses to explain ammonia toxicity on fish, some refer to oxygen transport and oxygen affinity of the blood. In fact, the partial pressure of oxygen in the blood (PaO2) decreases significantly for a lethal dose only. Moreover, the influence of ammonia on oxyphoric properties of red blood cells of Siberian sturgeon has been investigated in vivo (blood of fish exposed for 72 h to 4.5 mmol L−1 total ammonia, a lethal concentration) and in vitro (ammonia added to blood of control fish). Whatever the experimental conditions, ammonia did not modify the affinity of haemoglobin for oxygen illustrated by P50, Bohr effect, Hill number and percentage of methaemoglobin. Consequently, the toxicity of ammonia on Siberian sturgeon cannot be explained by an alteration of the gill morphology, the ionic exchanges or the oxygen-binding properties of the haemoglobin only.


Ammonia toxicity Gills morphology Ionic transfer PaO2 Oxygen affinity Siberian sturgeon Acipenser baerii 


  1. Abel PD, Skidmore JF (1975) Toxic effects of an anionic detergent on the gills of rainbow trout. Water Res 9:759–765CrossRefGoogle Scholar
  2. Ait-Fdil M (1986) Mise en évidence et propriétés des ATPases membranaires dans la branchie, les érythrocytes et le rein d’un Chondrostéen, l’esturgeon sibérien, A. baerii. Thèse N° 2157, Université Bordeaux I, p 60Google Scholar
  3. Benesch RE, Benesch R, Yung S (1973) Equations for the spectrometric analysis of haemoglobin mixtures. Anal Biochem 55:245–248CrossRefPubMedGoogle Scholar
  4. Bennouna M (1986) Equilibre hydrominéral du milieu intérieur et des érythrocytes chez un Chondrostéen, l’esturgeon sibérien, A. baerii au cours de variations expérimentales de salinité et de température de l’environnement. Thèse N° 2148, Université Bordeaux I, p 93Google Scholar
  5. Brockway DR (1950) Metabolic products and their effects. Prog Fish Cult 12:127–129CrossRefGoogle Scholar
  6. Bubien JK, Meade TL (1986) Electrophysiological abnormalities produced by ammonium in isolated perfused brook trout, Salvelinus fontinalis, hearts. J Fish Biol 28:47–53CrossRefGoogle Scholar
  7. Burggren WW, Randall DJ (1978) Oxygen uptake and transport during hypoxic exposure in the sturgeon Acipenser transmontanus. Respir Physiol 34:171–183CrossRefPubMedGoogle Scholar
  8. Busacker GP, Chavin W (1981) Characterization of Na+/K+ATPases and Mg2+ATPases from the gill and the kidney of the goldfish (Carassius auratus). Comp Biochem Physiol 69B:249–256Google Scholar
  9. Butler PJ, Metclalfe JD (1989) Cardiovascular and respiratory systems. In: Shuttleworth TJ (ed) Physiology of elasmobranch fishes. Berlin Springer, Verlag, pp 1–47Google Scholar
  10. Cameron JN (1973) Oxygen dissociation curves and content of blood from Alaskan burbot (Lota lota), pike (Esox lucius) and grayling (Thymallus arcticus). Comp Biochem Physiol A 46(3):491–496CrossRefPubMedGoogle Scholar
  11. Cameron JN, Heisler N (1983) Studies of ammonia in the rainbow trout: physico-chemical parameters, acid-base behavior and respiratory clearance. J Exp Biol 105:107–125Google Scholar
  12. Capuzzo JM (1988) Physiological effects of a pollutant gradient-introduction. Mar Ecol Prog Ser 46:111CrossRefGoogle Scholar
  13. Claiborne JB, Evans DH, Goldstein L (1982) Fish branchial Na+/NH4 + exchange is via basolateral Na+-K+-activated ATPases. J Exp Biol 96:431–434Google Scholar
  14. Crespo S, Nonnotte G, Colin DA, Leray C, Nonnotte L, Aubree A (1986) Morphological and functional alterations induced in trout intestine by dietary cadmium and lead. J Fish Biol 28:69–80CrossRefGoogle Scholar
  15. Daye PG, Garside ET (1976) Histopathological changes in surficial tissues of brook trout, Salvelinus fontinalis exposed to acute and chronic level of pH. Can J Zool 54:2140–2155Google Scholar
  16. Eddy FB (1973) Oxygen dissociation curves of blood of the tench, Tinca tinca. J Exp Biol 58:281–293Google Scholar
  17. Fromm PO, Gillette JR (1968) Effects of ambient ammonia on blood ammonia and nitrogen excretion of rainbow trout. Comp Biochem Physiol 26:887–896CrossRefPubMedGoogle Scholar
  18. Graham MS, Turner JD, Wood CM (1990) Control of ventilation in the hypercapnic skate Raja ocellata. I. Blood and extradural fluid. Respir Physiol 80:259–277CrossRefPubMedGoogle Scholar
  19. Haywood GP (1983) Ammonia toxicity in teleost fishes: a review. Can Tech Rep Fish Aquat Sei 1177:35 pGoogle Scholar
  20. Huertas M, Gisbert E, Rodríguez A et al (2002) Acute exposure of Siberian sturgeon (Acipenser baerii, Brandt) yearlings to nitrite: median-lethal concentration (LC50) determination, haematological changes and nitrite accumulation in selected tissues. Aquat Toxicol 57:257–266CrossRefPubMedGoogle Scholar
  21. Hunn JB, Christenson LM (1977) Chemical composition of blood and bile of the shovelnose sturgeon. Prog Fish Cult 39(2):59–61CrossRefGoogle Scholar
  22. Jensen FB (1990) Nitrite and red cell function in carp: control factors for nitrite entry, membrane potassium, ion permeation, oxygen affinity and methaemoglobin formation. J Exp Biol 152:149–166Google Scholar
  23. Jensen FB, Andersen NA, Heisler N (1987) Effects of nitrites exposure on blood respiratory properties, acid-base and electrolyte regulation in the carp, Cyprinus carpio. J Comp Physiol 157B:533–541CrossRefGoogle Scholar
  24. Lang T, Peters G, Hoffmann R, Meyer E (1987) Experimental investigations on the toxicity of ammonia: effects on ventilation frequency, growth, epidermal mucous cells and gill structure of rainbow trout Salmo gairdneri. Dis Aquat Org 3:159–165CrossRefGoogle Scholar
  25. Laurent P, Perry SF (1991) Environmental effects on fish gill morphology. Physiol Zool 64:4–65CrossRefGoogle Scholar
  26. Lavrova EA, Natochin YV, Shakhamatova EL (1984) Electrolytes in the tissues of sturgeon and bony fishes in fresh and salt water. J Ichthyol 24(5):156–160Google Scholar
  27. Leino RL, McCormick JH (1984) Morphological and morphometrical changes in chloride cells of the gills of Pimephales promelas after chronic exposure to acid water. Cell Tis Res 236:121–128CrossRefGoogle Scholar
  28. Leino RL, McCormick JH, Jensen KM (1987) Changes in gill histology of fathead minnows and yellow perch transferred to soft water or acidified soft water with particular reference to chloride cells. Cell Tis Res 250:389–399Google Scholar
  29. Lenfant C, Johansen (1966) Respiratory function in the elasmobranch Squalus sucklei. Respir Physiol 1:13–29CrossRefPubMedGoogle Scholar
  30. Maetz J (1973) Na+/NH4+, Na+/H+ exchanges and NH3 movement across the gill of Carassius auratus. J Exp Biol 58:255–275Google Scholar
  31. Maetz J, Garcia-Romeu F (1964) The mechanism of sodium and chloride uptake by the gill of a fresh water fish, Carassius auratus. J Gen Physiol 47:1209–1227Google Scholar
  32. Magnin E (1962) Recherches sur la systématique et la biologie des Acipenséridés. Ann Stn Centr Hydrobiol Appl 9:7–242Google Scholar
  33. Mallat J (1985) Fish gill structural changes induced by toxicants and other irritants; a statistical review. Can J Aquat Sci 42:630–648CrossRefGoogle Scholar
  34. Maxime V, Nonnotte G, Peyraud C, Williot P, Truchot JP (1995) Circulatory and respiratory effects of an hypoxic stress in the Siberian sturgeon. Respir Physiol 100:203–212CrossRefPubMedGoogle Scholar
  35. Mazeaud M, Mazeaud F, Donaldson EM (1977) Primary and secondary effects of stress in fish: some new data with a general review. Trans Am Fish Soc 106(3):201–212CrossRefGoogle Scholar
  36. Milligan CL, Wood CM (1987) Regulation of blood oxygen transport and red blood cell pHi after exhaustive activity in rainbow trout (Salmo gairdneri) and starry flounder (Platichthys stellatus). J Exp Biol 133:263–282PubMedGoogle Scholar
  37. Motais R, Guizouarn H, Garcia-Romeu (1991) Red cell volume regulation: the pivotal role of ionic strength in controlling swelling-dependent transport systems. Biochim Biophys Acta 1075:169–180CrossRefPubMedGoogle Scholar
  38. Natochin Y, Luk’yanenko VI, Lavrova YA, Metallov GF (1975) Cation contents of the blood serum during the marine and river periods in the life sturgeons. J Ichthyol 15(5):799–804Google Scholar
  39. Nikinmaa M (1982) The effects of adrenaline on the oxygen transport properties of Salmo gairdneri blood. Comp Biochem Physiol 71A:353–356Google Scholar
  40. Nonnotte G, Maxime V, Truchot JP, Williot P, Peyraud C (1993) Respiratory responses to progressive ambient hypoxia in the sturgeon, Acipenser baerii. Respir Physiol 91:71–82CrossRefPubMedGoogle Scholar
  41. Perry SF, Wood VM (1989) Control and coordination of gas transfer in fishes. Can J Zool 67:2961–2970CrossRefGoogle Scholar
  42. Potts WTW, Rudy PP (1972) Aspects of osmotic and ionic regulation in the sturgeon. J Exp Biol 56:703–715Google Scholar
  43. Robinette RH (1976) Effect of selected sub-lethal level of ammonia on the growth of channel catfish (Ictalurus punctatus). Prog Fish Cult 38(1):26–29CrossRefGoogle Scholar
  44. Salin D (1992) La toxicité de l’ammoniaque chez l’esturgeon sibérien, Acipenser baerii: effets morphologiques, physiologiques, métaboliques d’une exposition à des doses sblétales et létales. Thèse N° 749, Université Bordeaux I, p 134Google Scholar
  45. Salin D, Williot P (1991) Acute toxicity of ammonia to siberian sturgeon Acipenser baerii. In: Williot P (ed) Acipenser. Cemagref Publ, Anthony, France, pp 153–167Google Scholar
  46. Scott GR, Sloman KA (2004) The effects of environmental pollutants on complex fish behaviour: integrating behavioural and physiological indicators of toxicity. Aquat Toxicol 68(4):369–392CrossRefPubMedGoogle Scholar
  47. Segers JHL, Temmink JHM, Van den Berg JHL, Wegman RCC (1984) Morphological changes in the gill of carp (Cyprinus carpio L.) exposed to acutely toxic concentrations of methyl bromide. Water Res 18(11):1437–1441CrossRefGoogle Scholar
  48. Semenkova TB, Bayuna LV, Boev AA, Dyubin VP (1999) Effects of stress on serum cortisol levels of sturgeon in aquaculture. J Appl Ichthyol 15:270–272CrossRefGoogle Scholar
  49. Siegel S, Castellean NJ (1988) Non parametric statistics for the behavioral sciences. Mc Graw-Hill, Inc. 399pGoogle Scholar
  50. Skidmore JF, Towell PWA (1972) Toxic effects of zinc sulphate on the gills of rainbow trout. Water Res 6:217–230CrossRefGoogle Scholar
  51. Smart G (1976) The effect of ammonia exposure in gill structure of the rainbow trout (Salmo gairdneri). J Fish Biol 8:471–475CrossRefGoogle Scholar
  52. Smart G (1978) Investigation of the toxic mechanisms of ammonia to fish - gas exchange in rainbow trout (Salmo gairdneri) exposed to acutely lethal concentrations. J Fish Biol 12:93–104CrossRefGoogle Scholar
  53. Soivio A, Nikinma M (1981) The swelling of erythrocytes in relation to the oxygen affinity of the blood of the rainbow trout, Salmo gairdneri R. In: Pickering AD (ed) Stress and fish. Academic Press, London, pp 103–119Google Scholar
  54. Sousa RJ, Meade T (1977) The influence of ammonia on the oxygen delivery system of Coho salmon hemoglobin. Comp Physiol Biochem 58A:23–28Google Scholar
  55. Tetens V, Lykkeboe G (1981) Blood respiratory properties of rainbow trout, Salmo gairdneri: response to hypoxia acclimatation and anoxic incubation of blood in vitro. J Comp Physiol 145:117–125CrossRefGoogle Scholar
  56. Tetens V, Lykkeboe G (1985) Acute exposure of rainbow trout to mild and deep hypoxia: O2 affinity and O2 capacitance of arterial blood. Respir Physiol 61:221–235CrossRefPubMedGoogle Scholar
  57. Thurston RV, Russo RC, Luedtke RJ, Smith CE, Meyn EL, Chakoumakos C, Wang KC, Brown CJD (1984) Chronic toxicity of ammonia to rainbow trout. Trans Am Fish Soc 113:56–73CrossRefGoogle Scholar
  58. Tomasso JR, Davis KD, Simco BA (1981) Plasma corticosteroid dynamics in channel catfish (Ictalurus punctatus) exposed to ammonia and nitrite. Can J Fish Aquat Sci 38:1106–1112CrossRefGoogle Scholar
  59. Tucker VA (1967) Method for oxygen content and dissociation curves on microliter blood samples. J Appl Physiol 23:410–414CrossRefPubMedGoogle Scholar
  60. Tuurala H, Soivio A (1982) Structural and circulatory changes in the secondary lamellae of Salmo gairdneri gills after sub-lethal exposures to dehydroabietic acid and zinc. Aquat Toxicol 2:21–29CrossRefGoogle Scholar
  61. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol and Pharmacol 13(2):57–149CrossRefGoogle Scholar
  62. Velisek J, Svobodova Z, Machova J (2009) Effects of bifenthrin on some haematological, biochemical and histopathological parameters of common carp (Cyprinus carpio L.) Fish Physiol and Biochem 35(4):583–590CrossRefGoogle Scholar
  63. Weber RE, Lykkkeboe G (1978) Respiratory adaptations in carp blood: influence of hypoxia, red cell organic phosphates, divalent cations and CO2 on haemoglobin-oxygen affinity. J Comp Physiol 128:127–137CrossRefGoogle Scholar
  64. Wendelaar Bonga SE (1997) The stress response in fish. Physiological Review 77(3):591–625CrossRefGoogle Scholar
  65. Wobeser G (1975) Acute toxicity of methyl mercury chloride and mercuric chloride for rainbow trout (Salmo gairdneri) fry and fingerlings. J Fish Res Board Can 32:2005–2013CrossRefGoogle Scholar
  66. Wood CM, Mc Mahon DR, Donald M (1979) Respiratory gas exchange in the resting starry flounder, Platichthys stellatus: a comparison with other teleosts. J Exp Biol 78:167–179PubMedGoogle Scholar
  67. Yang HC, Chun SK (1986) Histopathological study of acute toxicity of ammonia on common car (Cyprinus carpio). Bull Koraen Fish Soc 19(3):249–256Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Guy Nonnotte
    • 1
  • Dominique Salin
    • 2
  • Patrick Williot
    • 3
  • Karine Pichavant-Rafini
    • 4
  • Michel Rafini
    • 5
  • Liliane Nonnotte
    • 1
  1. 1.La Teste de BuchFrance
  2. 2.Saint Médard en JallesFrance
  3. 3.AudengeFrance
  4. 4.Laboratoire ORPHY EA4324Université de Bretagne OccidentaleBrest Cedex 3France
  5. 5.Département Communication, Anglais, Sciences HumainesUniversité de Bretagne OccidentaleBrest Cedex 3France

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