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Fish Physiology and Biochemistry

, Volume 36, Issue 3, pp 741–747 | Cite as

Sex-related differences in aerobic capacities and reactive oxygen species metabolism in the silver eel

  • A. Amérand
  • A. Vettier
  • C. Moisan
  • M. Belhomme
  • P. Sébert
Article

Abstract

Silver European eels (Anguilla anguilla L.) need to develop important aerobic capacities to cope with their long fasting spawning migration at depth, particularly males which are about half the size of females. Moreover, they have to face potential oxidative stress because reactive oxygen species (ROS) production is linked to the increase in metabolic rate. Thus, aerobic metabolism was globally evaluated in male and female silver eels exposed to a 10.1 MPa hydrostatic pressure (1,000 m depth). Oxygen consumption (MO2), ROS production and antioxidant enzyme activities were measured in the muscle fibres. Males showed a trend in both higher rate of aerobic metabolism and ROS production than females. After pressure exposure, ROS production was inversely correlated to metabolic rate only in males. By facilitating MO2 rise with no harmful effects by ROS, the supposed enhanced aerobic capacities of males could speed up the sustained swimming. In females, the tendency to lower metabolic rate and higher catalase activity would make them less vulnerable to ROS effects. These results are in agreement with the hypothesis for different migration depths between genders.

Keywords

European eel migration Energy metabolism Reactive oxygen species Sex difference 

Notes

Acknowledgments

We thank Marie-Paule Friocourt for revision of the English. We are grateful to the EELREP European contract for partially funding this study.

References

  1. Aebi H (1984) Catalase in vitro. Meth Enzymol 105:121–126CrossRefGoogle Scholar
  2. Amérand A, Vettier A, Sébert P et al (2005) In vitro effect of hydrostatic pressure exposure on hydroxyl radical production in fish red muscle. Redox Rep 10:25–28CrossRefGoogle Scholar
  3. Belaud A, Barthelemy L, Peyraud C (1977) Temperature and per se hydrostatic pressure reversal of pentobarbital anesthesia in fish. J Appl Physiol 42:329–334CrossRefGoogle Scholar
  4. Bone Q (1978) Locomotor muscle. In: Hoar WS, Randall DJ (eds) Fish physiology, vol VII. Academic, New York, pp 321–349Google Scholar
  5. Chen Q, Vazquez EJ, Moghaddas S et al (2003) Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278:36027–36031CrossRefGoogle Scholar
  6. Dickson KA, Donley JM, Sepulveda C et al (2002) Effects of temperature on sustained swimming performance and swimming kinematics of the chub mackerel Scomber japonicus. J Exp Biol 205:969–980PubMedGoogle Scholar
  7. Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 2002(82):47–95CrossRefGoogle Scholar
  8. Dufour S, Fontaine YA (1985) La migration de reproduction de l’anguille européenne (Anguilla anguilla L.): rôle probable de la pression hydrostatique dans la stimulation de la fonction gonadotrope. Bull Soc Zool Fr 110:291–299Google Scholar
  9. Duine JM, Floch F, Cann-Moisan C et al (1998) Simultaneous measurement of monoamines, their metabolites and 2, 3- and 2, 5-dihydroxybenzoates by high-performance liquid chromatography with electrochemical detection. Application to rat brain dialysates. J Chromatogr B Biomed Sci Appl 716:350–353CrossRefGoogle Scholar
  10. Durif C, Dufour S, Elie P (2005) The silvering process of Anguilla anguilla: a new classification from the yellow resident to the silver migrating stage. J Fish Biol 66:1025–1043CrossRefGoogle Scholar
  11. Echtay KS, Brand MD (2007) 4-Hydroxy-2-nonenal and uncoupling proteins: an approach for regulation of mitochondrial ROS production. Redox Rep 12:26–28CrossRefGoogle Scholar
  12. Egginton S (1986) Metamorphosis of the American eel, Anguilla rostrata LeSeur: I. Changes in metabolism of skeletal muscle. J Exp Zool 237:173–184CrossRefGoogle Scholar
  13. Filho WD (2007) Reactive oxygen species, antioxidants and fish mitochondria. Front Biosci 12:1229–1237CrossRefGoogle Scholar
  14. Floyd RA, Watson JJ, Wong PK (1984) Sensitive assay of hydroxyl free radical formation utilizing high pressure liquid chromatography with electrochemical detection of phenol and salicylate hydroxylation products. J Biochem Biophys Methods 10:221–235CrossRefGoogle Scholar
  15. Hemmingsen A (1960) Energy metabolism as related to body size and respiratory surface, and its evolution. Rep Steno Hosp 9:453–456Google Scholar
  16. Indo HP, Davidson M, Yen HC et al (2007) Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 7:106–118CrossRefGoogle Scholar
  17. Ku HH, Brunk UT, Shoal RS (1993) Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic Biol Med 15:621–627CrossRefGoogle Scholar
  18. Letellier T, Malgat M, Coquet M et al (1992) Mitochondrial myopathy studies on permeabilized muscle fibers. Pediatr Res 32:17–22CrossRefGoogle Scholar
  19. Lewander K, Dave G, Johansson ML et al (1974) Metabolic and hematological studies on the yellow and silver phases of the European eel, Anguilla anguilla L. I. Carbohydrate, lipid, protein and inorganic ion metabolism. Comp Biochem Physiol 47(B):571–581Google Scholar
  20. Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175PubMedGoogle Scholar
  21. Owen SF (2001) Meeting energy budgets by modulation of behaviour and physiology in the eel (Anguilla anguilla L.). Comp Biochem Physiol 128(A):631–644Google Scholar
  22. Palstra A (2006) Energetic requirement and environmental constraints of reproductive migration and maturation of european silver eel (Anguilla anguilla L.). Thesis, University of Leiden, LeidenGoogle Scholar
  23. Pankhurst NW (1982a) Changes in body musculature with sexual maturation in the European eel Anguilla anguilla (L.). J Fish Biol 21:417–428CrossRefGoogle Scholar
  24. Pankhurst NW (1982b) Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla (L.). J Fish Biol 21:127–140CrossRefGoogle Scholar
  25. Saks VA, Veksler VI, Kuznetsov AV et al (1998) Permeabilized cell and skinned fiber techniques in studies of mitochondrial function in vitro. Mol Cell Biochem 184(20):81–100CrossRefGoogle Scholar
  26. Scaion D, Sébert P (2008) Glycolitic fluxes in European silver eel, Anguilla Anguilla: sex differences and temperature sensitivity. Comp Biochem Physiol 151(A):687–690CrossRefGoogle Scholar
  27. Sébert P, Barthelemy L (1985) Hydrostatic pressure and adrenergic drugs (agonists and antagonists): effects and interactions in fish. Comp Biochem Physiol 82(C):207–212Google Scholar
  28. Sébert P, Theron M (2001) Why can the eel, unlike the trout, migrate under pressure? Mitochondrion 1:79–85CrossRefGoogle Scholar
  29. Sébert P, Barthélémy L, Simon B (1990) Laboratory system enabling long-term exposure to hydrostatic pressure of fishes or other animals breathing water. Mar Biol 104:165–168CrossRefGoogle Scholar
  30. Sébert ME, Amérand A, Vettier A et al (2007) Effects of high hydrostatic pressure on the pituitary-gonad axis in the European eel. Anguilla anguilla (L.). Gen Comp Endocrinol 153:289–298CrossRefGoogle Scholar
  31. Sébert ME, Weltzien FA, Moisan C et al (2008) Dopaminergic systems in the European eel: characterization, brain distribution, and potential role in migration and reproduction. Hydrobiologia 602:27–46CrossRefGoogle Scholar
  32. Sébert P, Scaion D, Belhomme M (2009) High hydrostatic pressure improves the swimming efficiency of European migrating silver eel. Respir Physiol Neurobiol 165:112–114CrossRefGoogle Scholar
  33. Somero GN (1991) Hydrostatic pressure and adaptation to the deep sea. In: Prosser CL (ed) Environmental and metabolic animal physiology. WileyLiss, New York, pp 167–204Google Scholar
  34. Sugioka K, Shimosegawa Y, Nakano M (1987) Estrogens as natural antioxidants of membrane phospholipid peroxidation. FEBS Lett 210:37–39CrossRefGoogle Scholar
  35. Tesch FW (2003) The eel. Thorpe, OxfordCrossRefGoogle Scholar
  36. Theron M, Guerrero F, Sébert P (2000) Improvement in the efficiency of oxidative phosphorylation in the freshwater eel acclimated to 10.1 MPa hydrostatic pressure. J Exp Biol 203:3019–3023PubMedGoogle Scholar
  37. van den Thillart G, van Ginneken V, Korner F et al (2004) Endurance swimming of European eel. J Fish Biol 65:312–318CrossRefGoogle Scholar
  38. van Ginneken V, Maes G (2005) The European eel (Anguilla anguilla, Linnaeus), its lifecycle, evolution and reproduction: a literature review. Rev Fish Biol Fish 15:367–398CrossRefGoogle Scholar
  39. van Ginneken V, van den Thillart GE (2000) Eel fat stores are enough to reach the Sargasso. Nature 403:156–157CrossRefGoogle Scholar
  40. Veksler VI, Kuznetsov AV, Sharov VG et al (1987) Mitochondrial respiratory parameters in cardiac tissue: a novel method of assessment by using saponin-skinned fibers. Biochim Biophys Acta 892:191–196CrossRefGoogle Scholar
  41. Vettier A, Szekely C, Sébert P (2003) Are yellow eels from Lake Balaton able to cope with high pressure encountered during migration to the Sargasso sea? The case of energy metabolism. Anim Biol Leiden Neth 53:329–338CrossRefGoogle Scholar
  42. Vina J, Sastre J, Pallardo FV et al (2006) Role of mitochondrial oxidative stress to explain the different longevity between genders: protective effect of estrogens. Free Radic Res 40:1359–1365CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • A. Amérand
    • 1
  • A. Vettier
    • 1
    • 2
  • C. Moisan
    • 1
  • M. Belhomme
    • 1
  • P. Sébert
    • 1
  1. 1.EA 4324 ORPHY, UFR Sciences et Techniques, Université Européenne de BretagneUniversité de BrestBREST Cedex 3France
  2. 2.EA 2069, Unité de Recherche “Vignes et Vins de Champagne” Stress & Environnement, Laboratoire d’Eco-Toxicologie, UFR Sciences Exactes et NaturellesUniversité de REIMS Champagne-ArdenneReims Cedex 2France

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