Fish Physiology and Biochemistry

, Volume 26, Issue 2, pp 197–210 | Cite as

Production, release and olfactory detection of sex steroids by the tench (Tinca tinca L.)

  • M.L. Pinillos
  • A.I. Guijarro
  • M.J. Delgado
  • P.C. Hubbard
  • A.V.M. Canário
  • A.P. Scott


The present study is concerned with pheromone communication in tench (Tinca tinca L.), establishing firstly whether males have a high olfactory sensitivity to some typical teleost sex steroids and prostaglandins; and secondly whether males and females might be able to synthesise and release some of these steroids into the water. The C21 steroid, 17,20β-dihydroxy-4-pregnen-3-one (17,20β-P) was found to give large electro-olfactogram responses with an estimated threshold of detection of 10−12 M. The male tench were equally sensitive to glucuronidated 17,20β-P (10−11.6 M) but 100 times less sensitive to sulphated 17,20β-P (11−9.7 M). Preliminary data from cross-adaptation studies suggest that both the free and conjugated forms are detected by the same olfactory receptor(s). Male tench also had high olfactory sensitivity to prostaglandin F (PGF) and 15-keto PGF (11−11.5 and 10−11.4 M). They were relatively insensitive, however, to testosterone (T), androstenedione (AD), 11-ketotestosterone (11-KT), 17β-oestradiol (E2), 17,20β,21-trihydroxy-4-pregnen-3-one (17,20β,21-P) and 17,20α-dihydroxy-4-pregnen-3-one (17,20α-P). Radioimmunoassays were used to measure the steroids in plasma and water and all samples were processed for the measurement of free, sulphated and glucuronidated fractions. In females, free 17,20β-P, 17,20α-P, free and glucuronidated T, and AD in plasma showed the largest increases in response to injection with mammalian gonadotropin-releasing hormone analogue (GnRHa) or Ovaprim (a mixture of GnRHa and a dopamine inhibitor). Free 17,20β-P was released into the water at the greatest rate. Plasma concentrations of the two conjugated forms of 17,20β-P were also elevated 18 h after the administration of GnRHa, but not by as much as the free steroid. In males, AD and 11-KT showed the greatest increase in response to GnRHa and were moreover released into the water at a higher rate in the treated group than in the control. The data support a possible pheromonal role for free and glucuronidated 17,20β-P.

electro-olfactogram PGF 17,20β-P 17,20β-P-Glucuronide 17,20β-P-sulphate pheromone reproduction steroid teleost tench 


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  1. Appelt, C.W. and Sorensen, P.W. 1999. Freshwater fish release urinary pheromones in a pulsatile manner. In: Advances in Chemical Signals in Vertebrates. pp. 247–256. Edited by R.E. Johnston, D. Müller-Schwarze and P.W. Sorensen. Kluwer Academic/Plenum Publishers, New York.Google Scholar
  2. Becker, D., Galili, N. and Degani, G. 1992. GCMS-identified steroids and steroid glucuronides in gonads and holding water of Trichogaster trichopterus (Anabantidae, Pallas 1770). Comp. Biochem. Physiol. B 103: 15–19.CrossRefGoogle Scholar
  3. Bertmar, G. 1982. Structure and function of the olfactory mucosa of migrating Baltic trout under environmental stresses, with special reference to water pollution. In: Chemoreception in Fishes. pp. 395–422. Edited by T.J. Hara. Elsevier Scientific Publishing Company, Amsterdam.Google Scholar
  4. Billard, R., Fostier, A., Weil, C. and Breton, B. 1982. Endocrine control of spermatogenesis in teleost fish. Can. J. Fish. Aquat. Sci. 39: 65–79.Google Scholar
  5. Bjerselius, R. and Håkan Olsén, K. 1993. A study of the olfactory sensitivity of cruican carp (Carassius carassius) and goldfish (Carassius auratus) to 17α,20β-dihydroxy-4–pregnen-3–one and prostaglandin F2α. Chem. Sens. 18: 427–436.Google Scholar
  6. Breton, B., Horoszewicz, L., Bieniarz, K. and Epler, P. 1980a. Temperature and reproduction in tench: effect of a rise in the annual temperature regime on gonadotropin level, gametogenesis and spawning. I. The male. Reprod. Nutr. Develop. 20: 105–118.Google Scholar
  7. Breton, B., Horoszewicz, L., Bieniarz, K. and Epler, P. 1980b. Temperature and reproduction in tench: Effect of a rise in the annual temperature regime on gonadotropin level, gametogenesis and spawning. II. The female. Reprod. Nutr. Develop. 20: 1011–1024.Google Scholar
  8. Canario, A.V.M. and Scott, A.P. 1988. Structure-activity relationships of C21 steroids in an in vitro oocyte maturation bioassay in rainbow trout, Salmo gairdneri. Gen. Comp. Endocrinol. 71: 338–348.PubMedCrossRefGoogle Scholar
  9. Canario, A.V.M. and Scott, A.P. 1990. Effects of steroids and human chorionic gonadotrophin on in vitro oocyte final maturation in two marine flatfish: The dab, Limanda limanda and the plaice, Pleuronectes platessa. Gen. Comp. Endocrinol. 77: 171–176.Google Scholar
  10. Chang, C.-F. and Lee Y.-H. 1992. Purification of the sex-binding protein from common carp (Cyprinus carpio) plasma. Comp. Biochem. Physiol. B 101: 587–590.PubMedCrossRefGoogle Scholar
  11. Chang, J.P. and Peter, R.E. 1983. Effects of dopamine on gonadotropin release in female goldfish, Carassius auratus. Neuroendocrinology 36: 351–357.PubMedGoogle Scholar
  12. Crim, L.W., Peter, R.E. and Billard, R. 1981. Onset of gonadotropic hormone accumulation in the immature trout pituitary gland in response to estrogen or aromatizable steroid hormones. Gen. Comp. Endocrinol. 44: 374–381.PubMedCrossRefGoogle Scholar
  13. Defraipont, Mand Sorensen, P.W. 1993. Exposure to the pheromone 17α,20β-dihydroxy-4–pregnen-3–one enhances the behavioural spawning success, sperm production and sperm motility of male goldfish. Anim. Behav. 46: 245–256.CrossRefGoogle Scholar
  14. Dulka, J.L., Stacey, N.E., Sorensen, P.W. and Van Der Kraak, G.J. 1987. A steroid sex pheromone synchronizes male-female spawning readiness in goldfish. Nature 325: 251–253.CrossRefGoogle Scholar
  15. Ebrahimi, M., Scott, A.P. and Kime, D.E. 1996. Extragonadal production of 17,20–dihydroxy-4–pregnen-3–ones in vitro in cyprinid fish. Gen. Comp. Endocrinol. 104: 296–303.PubMedCrossRefGoogle Scholar
  16. Epler, P. Mejza, T. Bieniarz, K. and Sokolowska-Mikolajczyk, M. 1993. The effect of 17α hydroxy 20β dihydroprogesterone (17α 20β P) on carp and tench oocyte maturation in vitro and in vivo. Pol. Arch. Hydrobiol. 40: 197–207.Google Scholar
  17. Evans, R.E. and Hara, T.J. 1985. The characteristics of the electroolfactogram: its loss and recovery following olfactory nerve section in rainbow trout (Salmo gairdneri). Brain Res. 330: 65–75.PubMedCrossRefGoogle Scholar
  18. Goetz, F.W. 1983. Hormonal control of oocyte final maturation and ovulation in fishes. In: Fish Physiology. Vol. IXA, pp. 117–170. Edited by W.S. Hoar, D.J. Randall and E.M. Donaldson. Academic Press, New York.Google Scholar
  19. Greenwood, L.N., Scott, A.P., Vermeirssen, E.L.M., Fostier, A., Mylonas, C. and Pavlidis, M. 2001. Plasma steroids in mature common dentex (Dentex dentex) stimulated with a gonadotropin-releasing hormone agonist. Gen. Comp. Endocrinol. 123: 1–12.PubMedCrossRefGoogle Scholar
  20. Hobby, A.C. Pankhurst, N.W. and Geraghty, D.P. 2000. A comparison of sex steroid binding protein (SBP) in four species of teleost fish. Fish Physiol. Biochem. 23: 245–256.CrossRefGoogle Scholar
  21. Hubbard, P.C., Barata, E.N. and Canário, A.V.M. 2002. Possible disruption of pheromonal communication by humic acid in the goldfish, Carassius auratus. Aquat. Toxicol. 60: 169–183.PubMedCrossRefGoogle Scholar
  22. Idler, D.R., Fagerlund, U.H.M and Ronald, A.P. 1960. Isolation of pregnen-4–one 17,20–diol-3–one from the plasma of Pacific salmon. Biochem. Biophysic. Res. Com. 2: 133–137.CrossRefGoogle Scholar
  23. Irvine, I.A.S. and Sorensen, P.W. 1993. Acute olfactory sensitivity of wild common carp, Cyprinus carpio, to goldfish hormonal sex pheromones is influenced by gonadal maturity. Can. J. Zool. 71: 2199–2210.CrossRefGoogle Scholar
  24. Jalabert, B. 1976. In vitro oocyte maturation and ovulation in rainbow trout (Salmo gairdneri), northern pike (Esox lucius) and goldfish (Carassius auratus). J. Fish. Res. Board Can. 33: 974–988.Google Scholar
  25. Kitamura, S., Ogata, H. and Takashima, F. 1994. Olfactory responses of several species of teleost to F-prostaglandins. Comp. Biochem. Physiol. A 107: 463–467.Google Scholar
  26. Kobayashi, M., Aida, K. and Hanyu, I. 1989. Induction of gonadotropin surge by steroid hormone implantation in ovariectomized and sexually regressed female goldfish. Gen. Comp. Endocrinol. 73: 469–476.PubMedCrossRefGoogle Scholar
  27. Kouril, J. 1998. Hormonally induced spawning of tench Tinca tinca (L.) females. (A review). Pol. Arch. Hydrobiol. 45: 415–433.Google Scholar
  28. Laidley, C.W. and Thomas, P. 1994. Partial characterization of a sex-steroid binding protein in the spotted seatrout (Cynoscion nebulosus). Biol. Reprod. 51: 982–992.PubMedCrossRefGoogle Scholar
  29. Maren, T.H., Embry, R. and Broder, L.E. 1968. The excretion of drugs across the gills of the dogfish, Squalus acanthias. Comp. Biochem. Physiol. 26: 853–864.PubMedCrossRefGoogle Scholar
  30. Moore, A. and Scott, A.P. 1991. Testosterone is a potent odorant in precocious male Atlantic salmon (Salmo salar L.) parr. Philos. Trans. R. Soc. Lond. Ser. B 332: 241–245Google Scholar
  31. Moore, R.K., Scott, A.P. and Collins, P.M. 2000. Circulating C-21 steroids in relation to reproductive condition of a viviparous marine teleost, Sebastes rastrelliger (Grass Rockfish). Gen. Comp. Endocrinol. 117: 268–280.PubMedCrossRefGoogle Scholar
  32. Muus, B.J. and Dahlstrom, P. 1971. Collins guide to the freshwater fishes of Britain and Europe. Collins, London.Google Scholar
  33. Nagahama, Y. 1994. Endocrine regulation of gametogenesis in fish. Int. J. Dev. Biol. 38: 217–229.PubMedGoogle Scholar
  34. Nagahama, Y., Goetz, F.W. and Tan, J.D. 1986. Shift in steroidogenesis in the ovarian follicles of the goldfish (Carassius auratus) during gonadotropin-induced oocyte maturation. Dev. Growth Differ. 28: 555–561.CrossRefGoogle Scholar
  35. Peter, R.E., Chang, J.P., Nahorniak, C.S., Omeljaniuk, R.J., Sokolowska, M., Shih, S.H. and Billard, R. 1986. Interactions of catecholamines and GnRH in regulation of gonadotropin secretion in teleost fish. Recent Prog. Horm. Res. 42: 513–548.PubMedGoogle Scholar
  36. Pinillos, M.L., Delgado, M.J. and Scott, A.P. in press. Seasonal changes in plasma sex steroid concentration and gonadal morphology of tench, Tinca tinca. Aquac. Res.Google Scholar
  37. Poling, K.R., Fraser, E.J., and Sorensen, P.W. 2001. The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comp. Biochem. Physiol. B 129: 645–651.PubMedCrossRefGoogle Scholar
  38. Sakai, N., Iwamatsu, T., Yamauchi, K., Suzuki, N. and Nagahama, Y. 1988. Influence of follicular development on steroid production in the medaka (Oryzias latipes) ovarian follicle in response to exogenous substrates. Gen. Comp. Endocrinol. 71: 516–523.PubMedCrossRefGoogle Scholar
  39. Scott, A.P. and Canario A.V.M. 1987. Status of oocyte maturation-inducing steroids in teleost. In: Proc. 3rd Int. Symp. Reproductive Physiology of Fish. pp. 224–234. Edited by D.R. Idler, L.W. Crim and J.M. Walsh. Memorial University of Newfoundland, St John's.Google Scholar
  40. Scott, A.P. and Sorensen, P.W. 1994. Time course of release of pheromonally active gonadal steroids and their conjugates by ovulatory goldfish. Gen. Comp. Endocrinol. 96: 309–323.PubMedCrossRefGoogle Scholar
  41. Scott, A.P. and Vermeirssen, E.L.M. 1994. Production of conjugated steroids by teleost gonads and their role as pheromones. In: Perspectives in Comparative Endocrinology. pp. 645–654. Edited by K.G. Davey, R.E. Peter and S.S. Tobe. National Research Council of Canada, Otawa.Google Scholar
  42. Scott, A.P., Sumpter, J.P. and Hardiman, P.A. 1983. Hormone changes during ovulation in the rainbow trout (Salmo gairdneri Richarson). Gen. Comp. Endocrinol. 49: 128–134.PubMedCrossRefGoogle Scholar
  43. Scott, A.P., MacKenzie, D.S. and Stacey, N.E. 1984. Endocrine changes during natural spawning in the white sucker, Catostomus commersonii II. Steroid hormones. Gen. Comp. Endocrinol. 56: 349–359.PubMedCrossRefGoogle Scholar
  44. Scott, J.W. and Scott-Johnson, P.E. 2002. The electroolfactogram: a review of its history and uses. Microsc. Res. Tech. 58: 152–160.PubMedCrossRefGoogle Scholar
  45. Smith, R.L. 1973 The Excretory Function of Bile. Chapman and Hall, London.Google Scholar
  46. Sorensen, P.W. and Goetz, F.W. 1993. Pheromonal and reproductive function of F prostaglandins and their metabolites in teleost fish. J. Lipid Mediator. 6: 385–393.Google Scholar
  47. Sorensen, P.W., Hara, T.J, and Stacey, N.E. 1987. Extreme sensitivity of mature and gonadally regressed goldfish to a potent steroidal pheromone, 17α,20β-dihydroxy-4–pregnen-3–one. J. Comp. Physiol. A 160: 305–313.CrossRefGoogle Scholar
  48. Sorensen, P.W., Hara, T.J., Stacey, N.E. and Goetz, F.W.M. 1988. F prostaglandins function as a potent olfactory stimulus that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 39: 1039–1050.PubMedCrossRefGoogle Scholar
  49. Sorensen, P.W., Scott, A.P., Stacey, N.E. and Bowdin, L. 1995. Sulfated 17,20β-dihydroxy-4–pregnen-3–one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. Gen. Comp. Endocrinol. 100: 128–142.PubMedCrossRefGoogle Scholar
  50. Sorensen, P.W., Scott, A.P. and Kihslinger, R.L. 2000. How common hormonal metabolites function as relatively specific pheromonal signals in the goldfish. In: Proceedings of the 6th International Symposium on Reproductive Physiology of Fish, Bergen, Norway, July 4–9, 1999 (Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E. and Stefansson, S.O., Editors), pp. 125–128. Bergen 2000, Norway.Google Scholar
  51. Stacey, N.E. and Cardwell, J.R. 1995. Hormones as sex pheromones in fish. Widespread distribution among freshwater species. In: Proc. 5th Int. Symp. Reproductive Physiology of Fish. pp. 244–248. Austin, Texas.Google Scholar
  52. Stacey, N.E. and Cardwell, J.R. 1997. Hormonally-derived sex pheromone systems in fish: new approaches to controlled reproduction. In: Recent Advances in Marine Biotechnology, pp. 407–454. Edited by M. Fingerman, R. Nagabhushanam and M.F. Thompson. Oxford-IBH, New Delhi.Google Scholar
  53. Stacey, N.E. and Sorensen, P.W. 1986. 17α,20β-dihydroxy-4–pregnen-3–one: a steroidal primer pheromone increasing milt volume in the goldfish, Carassius auratus. Canad. J. Zool. 64: 2412–2417.CrossRefGoogle Scholar
  54. Stacey, N.E., Sorensen, P.W., Van Der Kraak, G.J. and Dulka, J.G. 1989. Direct evidence that 17α,20β-dihydroxy-4–pregnen-3–one functions as a goldfish primer pheromone: Preovulatory release is closely associated with male endocrine responses. Gen. Comp. Endocrinol. 75: 62–70.PubMedCrossRefGoogle Scholar
  55. Stacey, N.E., Sorensen, P.W., Dulka J.G., Cardwell, J.R. and Irvine, A.S. 1991. Fish sex pheromones: current status and potential applications. Bull. Inst. Zool. Academica Sinica Monogr. 16: 189–227.Google Scholar
  56. Stacey, N., Cardwell, J. and Murphy, C. 1996. Hormonal pheromones in freshwater fishes: Preliminary results of an electroolfactogram survey. In: Fish Pheromones: Origins and Modes of Action. pp. 47–55. Edited by A.V.M. Canario and D.M. Power. Universidade do Algarve, Faro.Google Scholar
  57. Steffens, W. 1995. The tench (Tinca tinca L.), a neglected pond fish species. Polskie Archiwum Hydrobiologii 42: 161–180.Google Scholar
  58. Trant, J.M. and Thomas, P. 1989. Isolation of a novel maturationinducing steroid produced in vitro by ovaries of Atlantic croaker. Gen. Comp. Endocrinol. 75: 397–404.PubMedCrossRefGoogle Scholar
  59. Van Den Hurk, R., Schoonen, W.G.E.J., Van Zoelen, G.A. and Lambert, J.G.D. 1987. The biosynthesis of steroid glucuronides in the testes of the zebrafish, Brachydanio rerio, and their pheromonal function as ovulation inducers. Gen. Comp. Endocrinol. 68: 179–188.PubMedCrossRefGoogle Scholar
  60. Van Weerd, J.H., Sukkel, M., Lambert, J.G.D. and Richter, C.J.J. 1991. GCMS-identified steroids and steroid glucuronides in ovarian growth stimulating holding water from adult African catfish, Clarias gariepinus. Comp. Biochem. Physiol. B 98: 303–311.CrossRefGoogle Scholar
  61. Vermeirssen, E.L.M. and Scott, A.P. 1996. Excretion of free and conjugated steroids in rainbow trout (Oncorhynchus mykiss): Evidence for branchial excretion of the maturation-inducing steroid, 17,20β-dihydroxy-4–pregnen-3–one. Gen. Comp. Endocrinol. 101: 180–194.PubMedCrossRefGoogle Scholar
  62. Wallace, R.A. 1985. Vitellogenesis and oocyte growth in nonmammalian vertebrates. In: Developmental Biology. pp. 127–177. Edited by L.W. Browder. Plenum Press, New York.Google Scholar
  63. Warren, J.C., Murdock G.L., Ma, Y., Goodman, S.R. and Zimmer, W.E. 1993. Molecular cloning of testicular 20β-Hydroxysteroid Dehydrogenase: Identity with aldose reductase. Biochemistry 32: 1401–1406.PubMedCrossRefGoogle Scholar
  64. Wheeler, A. 1978. Key to the Fishes of Northern Europe. Frederick Warne (Publishers) Ltd., London.Google Scholar
  65. Yamauchi, K., Kagawa, H., Ban, M., Kasahara N. and Nagahama, Y. 1984. Changes in plasma estradiol-17β and 17α,20ß-dihidroxy-4–pregnen-3–one levels during final oocyte maturation of the masu salmon, Oncorhynchus rhodurus. Bull. Jap. Soc. Sci. Fish. 50: 2137.Google Scholar
  66. Yoshikuni, M. and Nagahama, Y. 1991. Endocrine regulation of gametogenesis in fish. Bull. Inst. Zool. Academia Sinica 16: 139–172.Google Scholar
  67. Zheng, W., Strobeck, C. and Stacey, N.E. 1997. The steroid pheromone 17α,20β-dihydroxy-4–pregnen-3–one increases fertility and paternity in goldfish. J. Exp. Biol. 200: 2833–2840.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • M.L. Pinillos
    • 1
  • A.I. Guijarro
    • 1
    • 2
    • 3
  • M.J. Delgado
    • 2
    • 3
  • P.C. Hubbard
    • 3
  • A.V.M. Canário
    • 3
  • A.P. Scott
    • 1
  1. 1.The Centre for Environment, Fisheries and Aquaculture ScienceThe Nothe, Weymouth, DorsetUK
  2. 2.Departamento de Biología Animal II (Fisiología Animal), Facultad de BiologíaUniversidad ComplutenseMadridSpain
  3. 3.Centro de Ciências do MarUniversidade do AlgarveFaroPortugal

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