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Respiratory and Circulatory Responses to Hypoxia in the Sturgeon, Acipenser baerii

  • Guy Nonnotte
  • Patrick Williot
  • Valérie Maxime
Chapter

Abstract

Siberian sturgeon, Acipenser baerii, when exposed to progressive hypoxia, was able to maintain standard oxygen consumption until a low critical level of ambient PO2 (PwO2 < 40 mm Hg). During the post-hypoxic period, an O2 debt was repaid by an elevated oxygen consumption indicating that a shift to anaerobic metabolism had occurred during the exposure to severe hypoxia. Gradually increasing ambient hypoxia initially induced a respiratory alkalosis. Below the critical level of PwO2 and during normoxic recovery, a flush of lactate into the blood was associated with a metabolic acidosis which was totally compensated 3.5 h after return to normoxia. Respiratory responses of the sturgeon to progressive hypoxia reveal a typical O2 regulatory behavior.

An acute severe hypoxia (PwO2 = 10 mmHg) followed by a rapid return to normoxia caused a significant stress to the fish, as revealed by high levels of plasma catecholamines and cortisol. The moderate rise in heart rate and in dorsal aortic blood pressure observed during the first phase of hypoxia represented typical results of increased plasma catecholamines. These effects were then masked by a vagal reflex resulting in bradycardia. Deep hypoxia induced a hyperventilatory response followed by a marked ventilatory depression at the lowest level of PwO2. The initial ventilatory alkalosis was combined with a moderate metabolic acidosis. The latter was amplified during the first 2 h of the recovery period in normoxia, concomitantly with a flush of lactate into the blood and an increase in plasma sodium concentration. During normoxic recovery, hyperventilation resumed, consistent with the repayment of an oxygen debt.

Keywords

Siberian sturgeon Hypoxia Acid-base status O2 regulator Ventilation Circulation Heart rate Catecholamines Cortisol Fish 

Abbreviations

MO2

Standard oxygen consumption

PaO2

Oxygen partial pressure in arterial blood

PCO2

Carbon dioxide partial pressure

PO2

Oxygen partial pressure

PwO2

Oxygen partial pressure in water

αwO2

O2 solubility in water

Notes

Acknowledgments

We thank Dr. Karine Pichavant-Rafini (ORPHY laboratory, EA4324) and Michel Rafini (Professor at the Language Dpt) of the Brest University, for their kindness and constant availability and their help and scientific advices. Moreover, we are extremely indebted and grateful to them for the English corrections.

Notes of the Authors

These experiments were performed since 1990 to 1994. They have been investigated in the Laboratoire de Neurobiologie et Physiologie comparées, CNRS URA 1126 and the University of Bordeaux I, F-33120 Arcachon, in collaboration with the Laboratoire de Physiologie Animale, Brest University, F-29285 Brest and the IRSTEA (formerly CEMAGREF), F-33611 Cestas-Gazinet.

References

  1. Astrup P (1956) A simple electrometric technique for the determination of carbon dioxide tension in blood and plasma, total content of carbon dioxide in plasma and bicarbonate content in ‘separated’ plasma at a fixed dioxide tension (40 mmHg). Scand J Clin Invest 8:33–43CrossRefPubMedGoogle Scholar
  2. Boutilier RG, Dobson G, Hoeger U, Randall DJ (1988) Acute exposure to graded levels of hypoxia in rainbow trout (Salmo gairdneri): metabolic and respiratory adaptations. Respir Physiol 71:69–82CrossRefPubMedGoogle Scholar
  3. Boutilier RG, Iwama GK, Heming TA, Randall DJ (1985) The apparent pK of carbon acid in rainbow trout blood plasma between 5 and 15°C. Respir Physiol 61:237–254CrossRefPubMedGoogle Scholar
  4. Burggren WW, Randall DJ (1978) Oxygen uptake and transport during hypoxic exposure in the sturgeon Acipenser transmontanus. Respir Physiol 34:171–183CrossRefPubMedGoogle Scholar
  5. Burleson ML, Smatresk NJ (1990) Evidence for twO oxygen-sensitive chemoreceptor loci in channel catfish, Ictalurus punctatus. Physiol Zool 63(1):208–221CrossRefGoogle Scholar
  6. Dejours P (1981) Principles of comparative respiratory physiology. Elsevier, Amsterdam, New York, Oxford, p 265Google Scholar
  7. Donaldson EM (1981) The pituitary-interrenal axis as an indicator of stress in fish. In: Pickering AD (ed) Stress in fish. Academic press, New York, pp 11–47Google Scholar
  8. Duthie GG (1982) The respiratory metabolism of temperature-adapted flatfish at rest and during swimming activity and the use of anaerobic metabolism at moderate swimming speeds. J Exp Biol 97:259–373Google Scholar
  9. Forster ME (1981) Oxygen consumption and apnea in the shortfin eel, Anguilla australis schmidtii. New zeal. Aust J Mar Freshwat Res 15:85–90CrossRefGoogle Scholar
  10. Fritsche R, Nilsson S (1993) Cardiovascular and ventilatory control during hypoxia. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 180–206CrossRefGoogle Scholar
  11. Fry FEJ, Hart JS (1948) The relation of temperature to oxygen consumption in the goldfish. Biol Bull 94:66–77CrossRefPubMedGoogle Scholar
  12. Hipkins SF, Smith DG (1983) Cardiovascular events associated with spontaneous apnea in the australian short finned eel (Anguilla australis). J Exp Zool 227:339–348CrossRefGoogle Scholar
  13. Holeton GF, Randall DJ (1967) The effect of hypoxia upon the partial pressure of gases in the blood and water afferent and efferent to the gills of rainbow trout. J Exp Biol 46:317–327PubMedGoogle Scholar
  14. Hughes GM (1973) Respiratory response to hypoxia in fish. Am Zool 13:475–489CrossRefGoogle Scholar
  15. Iwama GK, McGeer JC, Pawluk MP (1989) The effects of five fish anaesthetics on acid-base balance, haematocrit, blood gases, cortisol and adrenaline in rainbow trout. Can J Zool 67:2065–2073CrossRefGoogle Scholar
  16. Klyashtorin LB (1981) The ability of sturgeons (Acipenseridae) to regulate gas exchange. J Ichthyol 21:141–144Google Scholar
  17. Le Moigne J, Soulier P, Peyraud-Waïtzenegger M, Peyraud C (1986) Cutaneous and gill O2 uptake in the European eel (Anguilla anguilla L.) in relation to ambient PO2, 10-400 mmHg. Respir Physiol 66:341–354CrossRefPubMedGoogle Scholar
  18. Lomholt JP, Johansen K (1979) Hypoxia acclimation in carp. How it affects O2 uptake, ventilation, and O2 extraction from water. Physiol Zool 52:38–49CrossRefGoogle Scholar
  19. Maruta K, Fugita K, Ito S, Nagatsu J (1984) Liquid chromatography of plasma catecholamines, with electro-chemical detection, after treatment with boric acid gel. Clin Chem 30:529–548Google Scholar
  20. Matty AJ (1985) The ‘adrenal’ and the kidney hormones. In: Fish endocrinology. Croom Helm Pub, London and Sydney, pp 112–137Google Scholar
  21. Maxime V, Peyraud-Waïtzenegger M, Claireaux G, Peyraud C (1990) Effect of rapid transfer from seawater to freshwater on respiratory variables, blood acid-base status and O2 affinity of hemoglobin in atlantic salmon (Salmo salar L.) J Comp Physiol B 160:31–39CrossRefGoogle Scholar
  22. Maxime V, Pennec J-P, Peyraud C (1991) Effects of direct transfer from freshwater to seawater on respiratory and circulatory variables and acid-base status in rainbow trout. J Comp Physiol B161(6):557–568Google Scholar
  23. Mazeaud MM, Mazeaud F (1981) Adrenergic responses in fish. In: Pickering AD (ed) Stress in fish. Academic Press, New York, pp 49–75Google Scholar
  24. Mazeaud MM, Mazeaud F, Donaldson EM (1977) Primary and secondary effects of stress in fish: some new data with general review. Trans Am Fish Soc 106(3):201–212CrossRefGoogle Scholar
  25. McDonald DG, Milligan CL (1992) Chemical properties of the blood. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish Physiol. Vol XII, part B. Academic Press, San Diego, pp 55–133Google Scholar
  26. McKenzie DJ, Taylor EW, Bronzi P, Bolis CG (1995) Aspects of cardioventilatory control in the Adriatic sturgeon (Acipenser naccarii). Respir Physiol 100:44–52CrossRefGoogle Scholar
  27. McKenzie DJ, Steffensen JF, Korsmeyer K, Whiteley NM, Bronzi P, Taylor EW (2007) Swimming alters response to hypoxia in the Adriatic sturgeon Acipenser naccarii. J Fish Biol 70:651–658CrossRefGoogle Scholar
  28. Metcalfe JD, Butler PJ (1989) The use of alpha-methyl-p-tyrosine to control circulating catecholamines in the dogfish Scyliorhinus canicula: the effects on gas exchange in normoxia and hypoxia. J Exp Biol 141:21–32Google Scholar
  29. Perry SF, Reid SD (1992) The relationship between beta-adrenoceptors and adrenergic responsiveness in trout (Oncorhynchus mykiss) and eel (Anguilla rostrata) erythrocytes. J Exp Biol 167:235–250PubMedGoogle Scholar
  30. Peyraud C (1965) Recherches sur la régulation des mouvements respiratoires chez quelques téléostéens: analyse du réflexe opto-respiratoire, Thèse de Doctorat ès Sciences, Université de Toulouse, p 258Google Scholar
  31. Peyraud C, Serfaty A (1964) Le rythme respiratoire de la carpe (Cyprinus carpio L.) et ses relations avec le taux de l’oxygène dissous dans le biotope. Hydrobiologia 23:165–178CrossRefGoogle Scholar
  32. Peyraud-Waitzenegger M, Barthelemy L, Peyraud C (1980) Cardiovascular and ventilatory effects of catecholamines in unrestrained eels (Anguilla anguilla L.) J Comp Physiol 138:367–375CrossRefGoogle Scholar
  33. Peyraud-Waitzenegger M, Savina A, Laparra J, Morfin R (1979) Blood-brain barrier for epinephrine in the eel (Anguilla anguilla L.) Comp Biochem Physiol 23(1):35–38Google Scholar
  34. Peyraud-Waïtzenegger M (1979) Simultaneous modifications of ventilation and arterial Po2 by catecholamines in the eel, Anguilla anguilla L.: participation of alpha and beta effects. J Comp Physiol B 129:343–354CrossRefGoogle Scholar
  35. Pickering AD, Pottinger TG, Sumpter JP, Carragher JF, Le Bail PY (1991) Effects of acute and chronic stress on the levels of circulating growth hormone in the rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 83:86–93CrossRefPubMedGoogle Scholar
  36. Prosser CL (1973) Comparative animal physiology, 3rd edn. Saunders, Philadelphia, p 966Google Scholar
  37. Randall DJ (1982) The control of respiration and circulation in fish during exercise and hypoxia. J Exp Biol 100:175–288Google Scholar
  38. Randall DJ, Perry SF (1992) Catecholamines. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish physiol. Vol XII, part B. Academic Press, San Diego, pp 255–300Google Scholar
  39. Randall DJ, McKenzie DJ, Abrami G, Bondiolotti GP, Natiello F, Bolis L, Agradi E (1992) Effect of diet on responses to hypoxia in sturgeon (Acipenser naccarii). J Exp Biol 170:113–125Google Scholar
  40. Randall DJ, Shelton G (1963) The effects of changes in environmental gas concentrations on the breathing and heart rate of a teleost fish. Comp Biochem Physiol 9:229–239CrossRefPubMedGoogle Scholar
  41. Ruer FM, Cech JJ, Doroshov SI (1987) Routine metabolism of the white sturgeon, Acipenser transmontanus: effect of population density and hypoxia. Aquaculture 62:45–52CrossRefGoogle Scholar
  42. 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 No 749, Université Bordeaux I, p 134Google Scholar
  43. Shelton G, Randall DJ (1962) The relation between heart beat and respiration in teleost fish. Comp Biochem Physiol 7:237–250CrossRefPubMedGoogle Scholar
  44. 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
  45. Thomas S, Kinkead R, Walsh PJ, WOod CM, Perry SF (1991) Desensitization of adrenaline-induced red blood cell H+ extrusion in vitro after chronic exposure of rainbow trout to moderate environmental hypoxia. J Exp Biol 156:233–248Google Scholar
  46. Truchot JP (1987) Comparative aspects of extracellular acid-base balance. In: Zoophysiology, vol 20. Springer Verlag, Berlin, Heidelberg, p 262Google Scholar
  47. Ultsch GR, Jackson DC, Moalli R (1981) Metabolic oxygen conformity among lower vertebrates: the toadfish revisited. J Comp Physiol B 142:439–443CrossRefGoogle Scholar
  48. Van Raij MTM, Van den Thillart GE, Vianen GJ, Pit DS, Balm PH, Steffens AB (1996) Substrate mobilization and hormonal changes in rainbow trout (Oncorhynchus mykiss) and common carp (Cyprinus carpio) during deep hypoxia and subsequent recovery. J Comp Physiol 166:443–452CrossRefGoogle Scholar
  49. Venkatesh B, Tan CH, Lam TJ (1989) Blood steroids in the goldfish: measurement of six ovarian steroids in small volumes of serum by reverse-phase high performance liquid chromatography and radioimmunoassay. Gen Comp Endocrinol 76:397–407CrossRefGoogle Scholar
  50. Vinberg GG (1956) Rate of metabolism and food requirements of fishes. Fisheries Research Board of Canada, Translation Series no 194, p 202Google Scholar
  51. Williot P, Comte S, Le Menn F (2011) Stress indicators throughout the reproduction of farmed Siberian sturgeon Acipenser baerii (Brandt) females. Intern Aquat Res 3:31–43Google Scholar
  52. Wood CM, Shelton G (1975) Physical and adrenergic factors affecting systemic vascular resistance in the rainbow trout: a comparison with branchial vascular resistance. J Exp Biol 63:505–523PubMedGoogle Scholar
  53. Wood CM, Shelton G (1980) Cardiovascular dynamics and adrenergic responses of the rainbow trout in vivo. J Exp Biol 87:247–270PubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Guy Nonnotte
    • 1
  • Patrick Williot
    • 2
  • Valérie Maxime
    • 3
  1. 1.La Teste de BuchFrance
  2. 2.AudengeFrance
  3. 3.Département Sciences de la Matière et de la VieUniversity of South BritainLorient-cedexFrance

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