Marine Biology

, Volume 150, Issue 6, pp 1417–1429 | Cite as

Effects of long-term acclimation to environmental hypercapnia on extracellular acid–base status and metabolic capacity in Mediterranean fish Sparus aurata

  • Basile Michaelidis
  • Anastasia Spring
  • Hans O. Pörtner
Research Article

Abstract

In the context of future scenarios of anthropogenic CO2 accumulation in marine surface waters, the present study addresses the effects of long-term hypercapnia on a Mediterranean fish, Sparus aurata. By equilibration with elevated CO2 levels seawater pH was lowered to a value of 7.3, close to the maximum pH drop expected in marine surface waters from atmospheric CO2 accumulation. Intra- and extracellular acid–base parameters as well as changes in enzyme profiles were studied in red and white muscles and the heart under both normocapnia and hypercapnia. The activities of pyruvate kinase (PK), lactate dehydrogenase (L-LDH), citrate synthase (CS), malate dehydrogenase and and 3-hydroxyacyl CoA dehydrogenase (HOAD) reflect the pathways and capacity of oxidative processes in metabolism. Long-term hypercapnia caused a transient reduction in blood plasma pH (pHe) as well as in intracellular pH (pHi). Compensation of the acidosis occurred through increased plasma and cellular bicarbonate levels. Changes in enzymatic activities, especially the increase in the activity of L-LDH, paralleled by a drop in CS activity in white and red muscles reflect a shift from aerobic to anaerobic pathways of substrate oxidation during long-term acclimation under hypercapnia. The present results suggest that moderate environmental hypercapnia changes the metabolic profile in tissues of S. aurata. Consequences for slow processes like growth and reproduction potential as well as potential harm at population, species and ecosystem levels require further investigation.

References

  1. Blancheton JP (2000) Developments in recirculation systems for Mediterranean fish species. Aquacult Eng 22:17–31CrossRefGoogle Scholar
  2. Burleson ML, Smatresk NJ (2000) Branchial chemoreceptors mediate ventilatory responses to hypercapnic acidosis in channel catfish. Comp Biochem Physiol 125A:403–414Google Scholar
  3. Burleson ML, Smatresk NJ, Milsom WK (1992) Afferent inputs associated with cardiovascular control in fish. In: Hoar WS, Randall DJ (eds) Fish Physiology. Academic, New York, pp 389–426Google Scholar
  4. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH Nature 425:365PubMedCrossRefGoogle Scholar
  5. Cameron JN (1971) Rapid method for determination of total carbon dioxide in small blood samples. J Appl Physiol 31:632–634PubMedGoogle Scholar
  6. Claiborne JB, Evans DE (1992) Acid–base balance and ion transfers in the spiny dogfish (Squalus acanthias) during hypercapnia: a role for ammonia excretion. J Exp Zool 261:9–17CrossRefGoogle Scholar
  7. Crocker EC, Cech Jr JJ (1998) Effects of hypercapnia on blood-gas and acid–base status in the white sturgeon, Acipenser transmontanus. J Comp Physiol 168B:50–60Google Scholar
  8. Cruz-Neto AP, Steffensen JF (1997) The effects of actute hypoxia and hypercapnia on oxygen consumption of the freshwater European eel. J Fish Biol 50:759–769CrossRefGoogle Scholar
  9. Driedzic RW, Almeida-Val VM F (1996) Enzymes of cardiac energy metabolism in Amazonian teleosts and fresh-water stingray (Potamotrygon hystrix). J Exp Zool 274:327–333CrossRefGoogle Scholar
  10. Driedzic RW, Sidell DB, Stowe D, Branscombe R (1987) Matching of vertebrate cardiac energy demand to energy metabolism. Am J Physiol 252:R930–R937PubMedGoogle Scholar
  11. Fivelstad S, Olsen AB, Klùften H, Ski H, Stefansson S (1999) Effects of carbon dioxide on Atlantic salmon (Salmo salar L.) smolts, at constant pH in bicarbonate rich freshwater. Aquaculture 178:171–187CrossRefGoogle Scholar
  12. Fivelstad S, Olsen AB, Åsgård T, Baeverfjord G, Rasmussen T, Vindheim T Stefansson S (2003) Longterm sublethal effects of carbon dioxide on Atlantic salmon smolts (Salmo salar L.): ion regulation, haematology, element composition, nephrocalcinosis and growth parameters. Aquaculture 215:301–319CrossRefGoogle Scholar
  13. Gilmour MK (2001) The CO2/pH ventilatory drive in fish. Comp Biochem Physiol A 130:219–240CrossRefGoogle Scholar
  14. Gilmour KM, Perry SF (1994) The effects of hypoxia, hyperoxia or hypercapnia on the acid–base disequilibrium in the arterial blood of rainbow trout. J Exp Biol 192:269–284PubMedGoogle Scholar
  15. Graham MS, Turner JD, Wood CM (1990) Control of ventilation in the hypercapnic skate Raja ocellata. I. Blood and extradural fluid. Respir Physiol 80:259–277PubMedCrossRefGoogle Scholar
  16. Hayashi M, Kita J, Ishimatsu A (2004) Acid–base responses to lethal aquatic hypercapnia in three marine fish. Mar Biol 144:153–160CrossRefGoogle Scholar
  17. Heisler N (1984) Acid–base regulation in fishes. In: Fish physiology Hoar WS, Randall DJ (eds) vol X, pp 315–392. Academic, OrlandoGoogle Scholar
  18. Heisler N (1986a) Comparative aspects of acid–base regulation. In: Heisler N (eds) Acid–base regulation in animals. Elsevier, AmsterdamGoogle Scholar
  19. Heisler N (1986b) Buffering and transmembrane ion transfer processes. In: Heisler N (eds).Acid–base regulation in animals. Elsevier, Amsterdam, pp 3–47Google Scholar
  20. Hochachka PW, Somero GN (2002) Biochemical adaptation. University Press, PrincetonGoogle Scholar
  21. Hughes GM, Shelton G (1962) Respiratory mechanisms and their nervous control in fish. Adv Comp Physiol Biochem 1:275–364PubMedGoogle Scholar
  22. Ibarz A, Fernadez-Borras J, Blasco J, Gallardo AM, Sanchez J (2003) Oxygen consumption and feeding rates of gilthead sea bream (Sparus aurata) reveal lack of acclimation to cold. Fish Physiol Biochem 29:313–321CrossRefGoogle Scholar
  23. International Panel on Climate Change (IPCC) (2001) Climate change: impacts, adaptations and vulnerability. Cambridge University Press, New YorkGoogle Scholar
  24. Ishimatsu A, Kita J (1999) Effects of environmental hypercapnia on fish. Jpn J Ichthyol 46:1–13Google Scholar
  25. Ishimatsu A, Kikkawa T, Hayashi M, Lee K-S, Kita J (2004) Effects of CO2 on marine fish: larvae and adults. J Oceanogr 60:731–741CrossRefGoogle Scholar
  26. Johnston IA, Moon TW (1980a) Endurance exercise training in the fast and slow muscles of a teleost fish (Pollachius virens). J Comp Physiol 135:147–156Google Scholar
  27. Johnston IA, Moon TW (1980b) Exercise training in skeletal muscle of brook trout (Salvelinus fontinalis). J Exp Biol 87:177–194Google Scholar
  28. Kinkead R, Perry SF (1991) The effects of catecholamines on ventilation in rainbow trout during hypoxia or hypercapnia. Respir Physiol 84:77–92PubMedCrossRefGoogle Scholar
  29. Lackner KSA (2003) A guide to CO2 sequestration. Science 300:1677–1678PubMedCrossRefGoogle Scholar
  30. Langenbuch M, Pörtner HO (2003) Energy budget of Antarctic fish hepatocytes (Pachycara brachycephalum and Lepidonotothen kempi) as a function of ambient CO2: pH dependent limitations of cellular protein biosynthesis? J Exp Biol 206:3895–3903PubMedCrossRefGoogle Scholar
  31. Larsen BK, Pörtner HO, Jensen FB (1997) Extra- and intracellular acid–base balance and ionic regulation in cod (Gadus morhua) during combined and isolated exposures to hypercapnia and copper. Mar Biol 128:337–346CrossRefGoogle Scholar
  32. Lee K-S, Kita J, Ishimatsu A (2003) Effects of lethal levels of environmental hypercapnia on cardiovascular and blood-gas status in yellowtail Seriola quinqueradiata. Zool Sci 20:417–422PubMedCrossRefGoogle Scholar
  33. Lowry OH, Passonneau JV (1972) A flexible system of enzymatic analysis. Academic, New YorkGoogle Scholar
  34. McKendry JE, Milsom WK, Perry SF (2001) Branchial CO2 receptors and cardiorespiratory ad- 2justments during hypercarbia in Pacific spiny dogfish (Squalus acanthias). J Exp Biol 204:1519–1527PubMedGoogle Scholar
  35. McKenzie DJ, Taylor WE, Dalla Valle ZA, Steffensen FJ (2002) Tolerance of acute hypercapnic acidosis by the European eel (Anguilla anguilla). J Comp Physiol 172B:339–B346Google Scholar
  36. Moon TW, Mommsen TP (1987) Enzymes of intermediary metabolism in tissues of little skate (Raja erinacea). J Exp Zool 244:9–15CrossRefGoogle Scholar
  37. Mozeto AA, Krusche AV, Luccas PO (1997) Aspectos do ciclo biogeoquimico do enoxfre em uma lagoa marginal da area alagavel do Rio Moji-Estacao Ecologica de Jatai, Luiz Antonio, SP. Geochem Brail 11:231–241Google Scholar
  38. Perry SF (1982) The regulation of hypercapnic acidosis in two salmonids, the freshwater trout (Salmo gairdneri) and the seawater salmon (Oncorhynchus kisutch). Mar Behav Physiol 9:73–79Google Scholar
  39. Perry SF, Reid SG (2002) Cardiorespiratory adjustments during hypercarbia in rainbow trout Oncorhynchus mykiss are initiated by external CO2 receptors on the first gill arch. J Exp Biol 202:2177–2190Google Scholar
  40. Perry SF, Walsh PJ, Mommsen TP, Moon TW (1988) Metabolic consequences of hypercapnia in the rainbow trout, Salmo gairdneri: b-adrenergic effects. Gen Comp Endocrinol 69:439–447PubMedCrossRefGoogle Scholar
  41. Pörtner HO (1990) An analysis of the effects of pH on oxygen binding by squid (Illexillecebrosus, Loligo pealei) haemocyanin. J Exp Biol 150:407–424Google Scholar
  42. Pörtner HO (2001) Climate change and temperature dependent biogeography: oxygen limitation of thermal tolerance in animals. Naturwissenschaften 88:137–146PubMedCrossRefGoogle Scholar
  43. Pörtner HO (2002) Climate change and temperature dependent biogeography: systemic to molecular hierarchies of thermal tolerance in animals. Comp Biochem Physiol 132A:739–761Google Scholar
  44. Pörtner HO, Boutilier GR, Tang Y, Towes PD (1990) Determination of intracellular pH and PCO2 after metabolic inhibition by fluoride and nitrilotriacetic acid. Resp Physiol 81:255–274CrossRefGoogle Scholar
  45. Pörtner HO, Reipschläger A, Heisler N (1998) Metabolism and acid–base regulation in Sipunculus nudus as a function of ambient carbon dioxide. J Exp Biol 201:43–55PubMedGoogle Scholar
  46. Pörtner HO, Bock C, Reipschläger A (2000) Modulation of the cost of pHi regulation during metabolic depression: a 31P-NMR study in invertebrate (Sipunculus nudus) isolated muscle. J Exp Biol 203:2417–2428PubMedGoogle Scholar
  47. Pörtner HO, Langenbuch M, Reipschläger A (2004) Biological impact of elevated ocean CO2 concentrations: lessons from animal physiology and earth history? J Oceanogr 60:705–718CrossRefGoogle Scholar
  48. Pörtner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of temperature extremes, hypoxia and increases in CO2 on marine animals: from earth history to global change. J Geophys Res—Oceans: 110, C09S10, doi: 10.1029/2004JC002561Google Scholar
  49. Reid GS, Sundin L, Kalinin AL, Rantin FT, Milsom WK (2000) Cardiovascular and respiratory reflexes in the tropical fish, traira (Hoplias malabaricus): CO2/pH chemoresponses. Resp Physiol 120:47–59CrossRefGoogle Scholar
  50. Ross RM, Krise WF, Redell LA, Bennett RM (2001) Effects of dissolved carbon dioxide on the physiology and behaviour of fish in artificial streams. Environ Toxicol 16:84–95PubMedCrossRefGoogle Scholar
  51. Sato T, Sato K (2002) Numerical prediction of the dilution process and its biological impacts in CO2 ocean sequestration. Mar Sci Technol 6:169–180CrossRefGoogle Scholar
  52. Scheid P, Shams H, Piiper J (1989) Gas exchange in vertebrates. Verh Dtsch Zool Ges 82:57–68Google Scholar
  53. Shirayama T, Thomton (2005) Effects of increased atmospheric CO2 on shallow-water marine benthos. J Geophys Res 110: C09S08, doi: 10.1029/2004JC002618Google Scholar
  54. Sidell BD, Driedzic WR, Stowe DB, Johnston IA (1987) Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol Zool 60:221–232Google Scholar
  55. Singer TD, Ballantyne JS (1989) Absence of extrahepatic lipid oxidation in a freshwater elasmobranch, the dwarf stingray (Potamotrygon megdalenae): evidence from enzyme activites. J Exp Zool 251:355–360CrossRefGoogle Scholar
  56. Smart GR, Knox D, Harrison JG, Ralph JA, Richards RH, Cowey CB (1979) Nephrocalcinosis in rainbow trout Salmo gairdneri Richardson; the effect of exposure to elevated CO2 concentration. J Fish Diseases 2:279–289CrossRefGoogle Scholar
  57. Söderström V, Nilsson EG (2000) Brain blood flow during hypercapnia in fish: no role of nitric oxide. Brain Res 857:207–211PubMedCrossRefGoogle Scholar
  58. Toews DP, Holeton GF, Heisler N (1983) Regulation of the acid–base status during environmental hypercapnia in the marine teleost fish Conger conger. J Exp Biol 107:9–20PubMedGoogle Scholar
  59. Tsikliras CA, Torre M, Stergiou IK (2005) Feeding habits and trophic level of round sardimella (Sardinella aurita) in the northeastern Mediterranean (Aegean Sea, Greece). J Biol Res 3:67–75Google Scholar
  60. Weber J-M, Haman F (1996) Pathways for Metabolic Fuels and Oxygen-in High Performance Fish. Comp Biochem Physiol 133A:33–38CrossRefGoogle Scholar
  61. Wedemeyer GA (1996) Physiology of fish in intensive culture systems. Chapman & Hall, New York, pp 60–98Google Scholar
  62. Wheatly MG (1989) Physiological response of the crayfish Pacifasticus leniusculus (Dana) to environmental hypoxia. I. Extracellular acid–base and electrolyte status and transbranchial exchange. J Exp Biol 57:673–680Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • Basile Michaelidis
    • 1
  • Anastasia Spring
    • 1
  • Hans O. Pörtner
    • 2
  1. 1.Laboratory of Animal Physiology, Department of Zoology, Faculty of Science, School of BiologyUniversity of ThessalonikiThessalonikiGreece
  2. 2.Alfred-Wegener-Institut für Polar-und Meeresforschung, Physiologie mariner TiereBremerhavenGermany

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