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Effects of Swimming on Silvering and Maturation of the European Eel, Anguilla anguilla L.

  • Arjan Palstra
  • Vincent van Ginneken
  • Guido van den Thillart
Part of the Fish & Fisheries Series book series (FIFI, volume 30)

Every year at the end of the growth season in autumn, the majority of the large European eels cease feeding, become restless and start to mature. Only those with sufficient lipid stores (Larsson et al. 1990; Svedäng and Wickström 1997) will start their reproductive migration to the spawning grounds in the Sargasso. They leave in a prepubertal condition with less than 2% relative gonad mass (GSI). The smaller males leave by August (Usui 1991). The large and fatty females leave between October and December to arrive an estimated 3.5 months later (Palstra et al. 2008a) at the spawning grounds. There, in early spring, males reach gonad masses of 10% and females of 40% to 60% of the body mass (Palstra et al. 2005). They are sexually mature and ready to spawn more than one million eggs (Van Ginneken et al. 2005).

As European eels have to swim about 5,500-km to reach their spawning site, swimming is supposed to play a crucial role in natural triggering and stimulation of maturation. Fine-tuning between migration and maturation of fishes is a non-elucidated research topic that deserves much more attention. It is peculiar that the influence of swim exercise on maturation has never been thoroughly investigated, especially since fatty migrant fishes like tuna and eel are of major commercial interest but very difficult or even impossible to reproduce in captivity.

Keywords

Fish Biol Lipid Mobilization FSHB Expression Dihydroxy Progesterone Hepatic Vitellogenesis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adachi S, Ijiri S, Kazeto Y, Yamauchi K (2003) Oogenesis in the Japanese Eel, Anguilla japonica. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel Biology. Springer, Tokyo, pp 502–518Google Scholar
  2. Barton BA, Schreck CB, Barton LD (1987) Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow trout. Dis Aquat Organ 2: 173–185CrossRefGoogle Scholar
  3. Boëtius I, Boëtius J (1967) Studies in the European Eel, Anguilla anguilla (L.). Experimental induction of the male sexual cycle, its relation to temperature and other factors. Meddelelser fra Danmarks Fiskeri- og Havundersogelser 4: 339–405Google Scholar
  4. Colombo G, Grandi G, Rossi R (1984) Gonad differentiation and body growth in Anguilla anguilla L. J Fish Biol 24: 215–228CrossRefGoogle Scholar
  5. Cottril RA, McKinley RS, Van der Kraak G, Dutil J-D, Reid KB, McGrath KJ (2001) Plasma non-esterified fatty acid profiles and 17β-oestradiol levels of juvenile immature and maturing adult American eels in the St Lawrence River. J Fish Biol 50: 364–379CrossRefGoogle Scholar
  6. Couillard CM, Hodson P V, Castonquay M (1997) Correlation between pathological changes and chemical contamination in American eels, Anguilla rostrata, from the St Lawrence River. Can J Fish Aquat Sci 54: 1916–1927CrossRefGoogle Scholar
  7. Davis K., Torrance P, Parker NC, Shuttle MA (1985) Growth, body composition and hepatic tyrosine aminotransferase activity in cortisol-fed channel catfish, Ictalurus punctatus. J Fish Biol 29: 177–184CrossRefGoogle Scholar
  8. DiBattista JD, Anisman H, Whitehead M, Gilmour KM (2005) The effects of cortisol administration on social status and brain monoaminergic activity in rainbow trout Oncorhynchus mykiss. J Exp Biol 208: 2707–2718PubMedCrossRefGoogle Scholar
  9. Dufour S, Fontaine YA (1985) La migration de reproduction de l'anguille européenne (Anguilla anguilla L.): un rôle probable de la pression hydrostatique dans la stimulation de fonction gonadotrope. B Soc Zool Fr 110: 291–299Google Scholar
  10. Dufour S, Burzawa-Gerard E, Le Belle N, Sbaihi M, Vidal B (2003) Reproductive endocrinology of the European eel, Anguilla anguilla. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel Biology. Springer, Tokyo, pp 373–386Google Scholar
  11. Durif C, Dufour S, Elie P (2005) The silvering process of the eel: a new classification from the yellow resident stage to the silver migrating stage. J Fish Biol 66: 1–19CrossRefGoogle Scholar
  12. Durif CMF, Dufour S, Elie P (2006) Impact of silvering stage, age, body size and condition on the reproductive potential of the European eel. Mar Ecol-Prog Ser, 327:171–181CrossRefGoogle Scholar
  13. EELREP (2005) Estimation of the reproduction capacity of European eel. Final report. http:// www.fishbiology.net/eelrepsum.html
  14. Endo T, Takashi T, Lokman MP, Ijiri S, Adachi S, Kohei Y (2007) In vitro induction of oil droplet accumulation into previtellogenic oocytes of Japanese eel, Anguilla japonica. Abstract book 8th International Symposium on Reproductive Physiology of Fish, June 3–8, Saint Malo, FranceGoogle Scholar
  15. Epstein FH, Cynamon M, McKay W (1971) Endocrine control of Na-K-ATPase in seawater adaptation in Anguilla rostrata. Gen Comp Endocrinol 16: 323–328CrossRefGoogle Scholar
  16. Fontaine YA (1994) L'argenture de l'anguille: métamorphose, anticipation, adaptation. B Fr Peche Piscic 335: 171–186CrossRefGoogle Scholar
  17. Freeman HC, Idler DR (1973) Effects of corticosteroids on liver transaminases in two salmonids, the rainbow trout (Salmo gairdneri) and the brook trout (Salvelinus fontinalis). Gen Comp Endocrinol 20: 69–76PubMedCrossRefGoogle Scholar
  18. Huang Y, Rousseau K, Sbaihi M, Le Belle N, Schmitz M, Dufour S (1999) Cortisol selectively stimulates pituitary gonadotropin β-subunit in a primitive teleost, Anguilla anguilla. Endocrinology 130: 1228–1235CrossRefGoogle Scholar
  19. Huertas M, Scott AP, Hubbard PC, Canario AV, Cerda J (2006) Sexually mature European eels (Anguilla anguilla L.) stimulate gonadal development of neighbouring males: possible involvement of chemical communication. Gen Comp Endocrinol 147 (3): 304–313PubMedCrossRefGoogle Scholar
  20. Kagawa H, Iinuma N, Tanaka H, Ohta H, Okuzawa K (1998) Effects of rearing period in seawater on induced maturation in female Japanese eel Anguilla japonica. Fish Sci 64: 77–82Google Scholar
  21. Kagawa H (2003) Artificial induction of oocyte maturation and ovulation. In: Aida K, Tsukamoto K, Yamauchi K (eds). Eel Biology. Springer, Tokyo, pp 401–414Google Scholar
  22. Kagawa H, Tanaka H, Ohta H, Unuma T, Nomura K (2005) The first success of glass eel production in the world: basic biology on fish reproduction advances new applied technology in aquaculture. Fish Physiol Biochem 31: 193–199CrossRefPubMedGoogle Scholar
  23. Kamei H, Kawazoe I, Kaneko T, Aida K (2005) Purification of follicle-stimulating hormone from immature Japanese eel, Anguilla japonica, and its biochemical properties and steroidogenic activities. Gen Comp Endocrinol 143 (3): 257–266PubMedCrossRefGoogle Scholar
  24. Kamei H, Kaneko T, Aida K (2006) Steroidogenic activities of follicle-stimulating hormone in the ovary of Japanese eel, Anguilla japonica. Gen Comp Endocrinol 146 (2): 83–90PubMedCrossRefGoogle Scholar
  25. Kazeto Y, Ijiri S, Adachi S, Yamauchi K (2006) Cloning and characterization of a cDNA encoding cholesterol side-chain cleavage cytochrome P450 (CYP11A1): Tissue distribution and changes in the transcript abundance in ovarian tissue of Japanese eel, Anguilla japonica, during artificially induced sexual development. J Steroid Biochem 99 (2–3): 121–128CrossRefGoogle Scholar
  26. Kwon HC, Choi SH, Kim YU, Son SO, Kwon JY (2005) Androgen action on hepatic vitellogenin synthesis in the eel, Anguilla japonica is suppressed by an androgen receptor antagonist. J Steroid Biochem 96 (2): 175–178CrossRefGoogle Scholar
  27. Lam TJ (1983) Environmental influences on gonadal activity in fish. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish Physiology. Volume IX. Reproduction. Part B Behaviour and Fertility Control. Academic, New York, pp 65–116Google Scholar
  28. Larsson P, Hamrin S, Okla L (1990) Fat content as a factor inducing migratory behaviour in the eel (Anguilla anguilla L.) to the Sargasso Sea. Naturwissenschaften 77: 488–490CrossRefGoogle Scholar
  29. Lethimonier-Desdoits C, Flouriot G, Valotaire Y, Kah O, Ducouret B (2000) Transcriptional interference between glucocorticoid receptor and estradiol receptor mediates the inhibitory effect of cortisol on fish vitellogenesis. Biol Reprod 62: 1763–1777CrossRefGoogle Scholar
  30. Li Y-Y, Inoue K, Takei Y (2003) Steroidgenic acute regulatory protein in eels: cDNA cloning and effects of ACTH and seawater transfer on its mRNA expression. Zool Sci 20: 211–219PubMedCrossRefGoogle Scholar
  31. Liley NR, Stacey NE (1983) Hormones, pheromones, and reproductive behaviour in fish. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish Physiology. Volume IX. Reproduction. Part B Behaviour and Fertility Control. Academic, New York, pp. 1–64Google Scholar
  32. Lokman PM, Rohr DH, Davie PS, Young G (2003) The physiology of silvering in anguillid eels: androgens and control of metamorphosis from the yellow to silver stage. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel Biology. Springer, Tokyo, pp. 331–350Google Scholar
  33. Mills D (1989) Ecology and Management of Atlantic Salmon. Chapman & Hall, LondonGoogle Scholar
  34. Miura T, Miura C, Yamauchi K (2003) Spermatogenesis in the Japanese eel. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel Biology. Springer, Tokyo, pp. 319–330Google Scholar
  35. Mommsen TP, Vijayan MM, Moon TW 1999. Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fisher 9: 211–268CrossRefGoogle Scholar
  36. Nagae M, Adachi S, Yamauchi K (1993) Changes in transcription of pituitary glycoprotein hormone and gonadotropin IIβ subunits during ovarian development induced by repeated injections of salmon pituitary homogenate in the Japanese eel, Anguilla japonica. Fish Physiol Biochem 17: 179–186CrossRefGoogle Scholar
  37. Nilsson L, Nyman L, Westin L, Ornhagen H 1981. Simulation of the reproductive migration of European eels (Anguilla anguilla (L.)) through manipulation of some environmental factors under hydrostatic compression. Speculat Sci Technol 4 (5): 475–484Google Scholar
  38. Olivereau M, Olivereau J (1979) Effects of estradiol-17β on the cytology of the liver, gonads and pituitary, and on plasma electrolytes in the female fresh-water eel. Cell Tissue Res 199: 431–454PubMedCrossRefGoogle Scholar
  39. Palstra AP, de Graaf M, Sibbing FA (2004) Riverine spawning and reproductive segregation in a lacustrine cyprinid species flock, facilitated by homing? Anim Biol 54 (4): 393–416CrossRefGoogle Scholar
  40. Palstra AP, Cohen EGH, Niemantsverdriet PRW, Van Ginneken VJT, Van den Thillart, GEEJM (2005) Artificial maturation and reproduction of European silver eel: Development of oocytes during final maturation. Aquaculture 249 (1–4): 533–547CrossRefGoogle Scholar
  41. Palstra A (2006) Energetic requirements and environmental constraints of reproductive migration and maturation of European silver eel (Anguilla anguilla L.). Ph.D. thesis, University of Leiden, Leiden, The NetherlandsGoogle Scholar
  42. Palstra AP, Antonissen E, Clavero ME, Nieveen M, Niemantsverdriet P, Van Ginneken VJT, Van den Thillart GEEJM (2006a) The fate of fat in silver eels: lipid requirements for spawning migration. In: Palstra AP (ed) Energetic Requirements and Environmental Constraints of Reproductive Migration and Maturation of European Silver Eel (Anguilla Anguilla L.). Ph.D. thesis University of Leiden, LeidenGoogle Scholar
  43. Palstra AP, Van Ginneken VJT, Murk AJ, Van den Thillart GEEJM (2006b) Are dioxin-like contaminants responsible for the eel (Anguilla anguilla) drama? Naturwissenschaften 93: 145–148CrossRefGoogle Scholar
  44. Palstra A, Curiel D, Fekkes M, de Bakker M, Székely C, Van Ginneken V, Van den Thillart G (2007a) Swimming stimulates oocyte development in European eel (Anguilla anguilla L.). Aquaculture 270: 321–332CrossRefGoogle Scholar
  45. Palstra AP, Heppener DFM, Van Ginneken VJT, Székely C, Van den Thillart GEEJM (2007b) Swimming performance of silver eels is severely impaired by the swim-bladder parasite Anguillicola crassus. J Exp Mar Biol Ecol. 352: 244–256CrossRefGoogle Scholar
  46. Palstra A, Schnabel D, Nieveen M, Spaink H, Van den Thillart G (2007c) Swimming increases gonadotropin sensitivity of European female silver eels as shown by q-PCR of the estradiol receptor and vitellogenin in the liver. Abstract book 8th International Symposium on Reproductive Physiology of Fish, June 3–8, Saint Malo, FranceGoogle Scholar
  47. Palstra A, van Ginneken V, van den Thillart G (2008a) Cost of transport and optimal swimming speeds in farmed and wild European silver eels (Anguilla anguilla). Comp Biochem Physiol. Part A 151: 37–44CrossRefGoogle Scholar
  48. Palstra AP, Schnabel D, Nieveen MC, Spaink HP, van den Thillart GEEJM (2008b) Male silver eels mature by swimming. BMC Physiology 8: 14CrossRefGoogle Scholar
  49. Pankhurst NW (1982) Relation of visual changes to the onset of sexual maturation in the European eel Anguilla anguilla L. J Fish Biol 21: 127–140CrossRefGoogle Scholar
  50. Patterson DA, MacDonald JS, Hinch SG, Healey MC, Farrell AP (2004) The effect of exercise and captivity on energy partitioning, reproductive maturation and fertilization success in adult sockeye salmon. J Fish Biol 64: 1039–1059CrossRefGoogle Scholar
  51. Pedersen BH (2003) Induced sexual maturation of the European eel Anguilla anguilla and fertilisation of the eggs. Aquaculture 224: 323–338CrossRefGoogle Scholar
  52. Pedersen BH (2004) Fertilisation of eggs, rate of embryonic development and hatching following induced maturation of the European eel Anguilla anguilla. Aquaculture 237: 461–473CrossRefGoogle Scholar
  53. Petersen I, Korsgaard B (1989) Experimental induction of vittelogenin synthesis in eel (Anguilla anguilla) adapted to sea-water or fresh-water. Comp Biochem Physiol 93B: 57–60Google Scholar
  54. Peyon P, Baloche S, Burzawa-Gerard E (1993) Synthesis of vittelogenin by eel (Anguilla anguilla L.) hepatocytes in primary culture: requirement of estradiol-17β priming. Gen Comp Endocrinol 91: 318–329PubMedCrossRefGoogle Scholar
  55. Robins CR, Cohen DM, Robins CH (1979) The eels Anguilla and Histiobranchus, photographed on the floor of the deep Atlantic in the Bahamas. Bull Mar Sci 29: 401–405Google Scholar
  56. Rohr DH, Lokman PM, Davie PS, Young G (2001) 11-Ketotestosterone induces silvering-related changes in immature female short-finned eels, Anguilla australis. Comp Biochem Physiol 130A: 701–714Google Scholar
  57. Sato N, Kawazoe I, Suzuki Y, Aida K (2003) Induction of vitellogenesis. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel Biology. Springer, Tokyo, pp. 387–399Google Scholar
  58. Saito K, Lokman PM, Young G, Ozaki Y, Matsubara H, Okumura H, Kazeto Y, Yoshiura Y, Aida K, Adachi S, Yamauchi K (2003) Follicle-stimulating hormone β, luteinizing hormone β and glyco-protein hormone α subunit mRNA levels in artificially maturing Japanese eel Anguilla japonica and naturally maturing New Zealand longfinned eel Anguilla dieffenbachia. Fish Sci 69: 146–153CrossRefGoogle Scholar
  59. Sbaihi M, Fouchereau-Perron M, Meunier F, Elie P, Mayer I, Burzawa-Gerard E, Vidal B, Dufour S (2001) Reproductive biology of the conger eel from the south coast of Brittany, France and comparison with the European eel. J Fish Biol 59: 302–318Google Scholar
  60. Sbaihi M (2002) Interaction des steroïdes sexuels et du cortisol dans le contrôle de la fonction de reproduction et du métabolisme calcique chez un Téléostéen migrateur, l'anguille (Anguilla anguilla L.). Cybium 2002: 26 (1): 64Google Scholar
  61. Sbaihi M, Kacem A, Aroua S, Baloche S, Rousseau K, Lopez E, Meunier F, Dufour S (2007) Thyroid hormone-induced demineralisation of the vertebral skeleton of the eel, Anguilla anguilla. Gen Comp Endocrinol 151: 98–107PubMedCrossRefGoogle Scholar
  62. Schmitz M, Aroua S, Vidal B, Le Belle N, Elie P, Dufour S (2005) Differential Regulation of Luteinizing Hormone and Follicle-Stimulating Hormone Expression during Ovarian Development and under Sexual Steroid Feedback in the European Eel. Neuroendocrinology 81: 107–119PubMedCrossRefGoogle Scholar
  63. Sébert M-E, Vettier A, Dufour S, Amerand A, Baloche S, Weltzien FA, Sébert P (2005) Mimicking environmental conditions of European eel oceanic migration: effects of exposure to high hydrostatic pressure on the brain-pituitary-gonad axis. Fish and Diadromy in Europe. Ecology, Management, Conservation. Bordeaux 29 March–1 April 2005Google Scholar
  64. Sébert M-E, Amerand A, Vettier A, Weltzien FA, Pasqualini C, Sébert P, Dufour S (2007) Effects of high hydrostatic pressure on the pituitary-gonad axis in the European eel, Anguilla anguilla (L.). Gen Comp Endocrinol. 153: 289–298PubMedCrossRefGoogle Scholar
  65. Stocco DM (2001) StAR protein and the regulation of steroid hormone biosynthesis. Ann Rev Physiol 63: 193–213CrossRefGoogle Scholar
  66. Suetake H, Okubo K, Sato N, Yoshiura Y, Suzuki Y, Aida K (2002) Differential expression of two gonadotropin (GTH) β subunit genes during ovarian maturation induced by repeated injection of salmon GTH in the Japanese eel Anguilla japonica. Fish Sci 68: 290–298CrossRefGoogle Scholar
  67. Suetake H, Okubo K, Yoshiura Y, Aida K (2003) GTH and GnRH molecules and their expression in the Japanese eel. In: Aida K, Tsukamoto K, Yamauchi K (eds) Eel Biology. Springer, Tokyo, pp. 351–372Google Scholar
  68. Svedäng H, Wickström H (1997) Low fat contents in female silver eels: indications of insufficient energetic stores for migration and gonadal development. J Fish Biol 50: 475–486CrossRefGoogle Scholar
  69. Tesch FW (2003) The Eel. Blackwell Science, OxfordGoogle Scholar
  70. Todd PR (1981) Morphometric changes, gonad histology, and fecundity estimates in migrating New Zealand fresh-water eels (Anguilla spp.). N Z J Mar Freshw Res 15: 155–170CrossRefGoogle Scholar
  71. Usui A (1991) Eel Culture. Blackwell Scientific Publications Ltd, LondonGoogle Scholar
  72. Van den Thillart G, Van Ginneken V, Körner F, Heijmans R, Van der Linden R, Gluvers A (2004) Endurance swimming of European eel. J Fish Biol 65: 1–7Google Scholar
  73. Van Ginneken VJT, Maes GE (2005) The European eel (Anguilla anguilla Linnaeus), its lifecycle, evolution and reproduction: a literature review. Rev Fish Biol Fisher 15: 367–398CrossRefGoogle Scholar
  74. Van Ginneken V, Vianen G, Muusze B, Palstra A, Verschoor L, Lugten O, Onderwater M, Van Schie S, Niemantsverdriet P, Van Heeswijk R, Eding E, Van den Thillart G (2005) Gonad development and spawning behaviour of artificially-matured European eel (Anguilla anguilla L.). Anim Biol 55 (3): 203–218CrossRefGoogle Scholar
  75. Van Ginneken V, Durif C, Dufour S, Sbaihi M, Boot R, Noorlander K, Doornbos J, Palstra A, Goos H, Antonissen E, Mayer I, Van den Thillart G (2007a) A 5,500-km swim trial stimulates gonad maturation in the European eel (Anguilla anguilla L.). Comp Biochem Physiol. Part A 147: 1095–1103CrossRefGoogle Scholar
  76. Van Ginneken V, Durif C, Balm SP, Boot R, Verstegen MWA, Antonissen E, Van den Thillart G (2007b) Silvering of European eel (Anguilla anguilla L.): Seasonal changes of morphological and metabolic parameters. Anim Biol 57 (1): 63–77CrossRefGoogle Scholar
  77. Verslycke T, Vandenbergh GF, Versonnen B, Arijs K, Janssen CR (2002). Induction of vitellogen-esis in 17α-ethinylestradiol-exposed rainbow trout (Oncorhynchus mykiss): a method comparison. Comp Biochem Physiol. Part C 132: 483–492Google Scholar
  78. Versonnen BJ, Goemans G., Belpaire C, Janssen CR (2004). Vitellogenin content in European eel (Anguilla anguilla) in Flanders, Belgium. Environ Pollut 128 (3): 363–371PubMedCrossRefGoogle Scholar
  79. Vidal B, Pasqualini C, Le Belle N, Claire M, Holland H, Sbaihi M, Vernier P, Zohar Y, Dufour S (2004) Dopamine inhibits luteinizing hormone synthesis and release in the juvenile European eel: A neuroendocrine lock for the onset of puberty. Biol Reprod 71: 1491–1500PubMedCrossRefGoogle Scholar
  80. Weltzien F-A, Pasqualini C, Sébert M-E, Vidal B, Le Belle N, Kah O, Vernier P, Dufour S (2006) Androgen-Dependent Stimulation of Brain Dopaminergic Systems in the Female European Eel (Anguilla anguilla). Endocrinology 147 (6): 2964–2973PubMedCrossRefGoogle Scholar
  81. Yaran Z, Cocos M, Salzer H (1980) Effects of temperature and photoperiod on ovarian recrudescence in the cyprinid fish Mirogrex terrae-sanctae. J Fish Biol 16: 371–382CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media B.V 2009

Authors and Affiliations

  • Arjan Palstra
    • 1
  • Vincent van Ginneken
    • 1
  • Guido van den Thillart
    • 1
  1. 1.Integrative ZoologyInstitute of Biology Leiden Van der Klaauw LaboratoriesRA LeidenThe Netherlands

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