Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes

Fish Physiology and Biochemistry

Volumn 26, Issue 1, 2002, Pages 13-29

  Strüssmann, Carlos Augusto ^a   Nakamura, Masaru ^b  

^a TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

^b UNIVERSITY OF THE RYUKYUS   (Japan)

Author keywords

Environment; Fish; Sex determination; Sex differentiation; Steroidogenesis

Indexed keywords

SEX HORMONE;

ENDOCRINE FUNCTION; ENDOCRINOLOGY; ENVIRONMENTAL FACTOR; ENVIRONMENTAL PARAMETERS; ENVIRONMENTAL TEMPERATURE; FISH; FISHERY; FOOD INDUSTRY; GENETIC REGULATION; GENOTYPE; GONAD DEVELOPMENT; HORMONE SYNTHESIS; MORPHOLOGY; NONHUMAN; OVARY DEVELOPMENT; REVIEW; SENSITIVITY ANALYSIS; SEX DETERMINATION; SEX DIFFERENTIATION; STEROIDOGENESIS; TELEOST; TESTIS DEVELOPMENT;

PISCES; TELEOSTEI;

EID: 18744427525     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1023343023556     Document Type: Review

References (100)

1. Afonso, L.O.B., Wassermann, G.J. and Oliveira, R.T. 2001. Sex reversal in Nile tilapia (Oreochromis niloticus) using a nonsteroidal aromatase inhibitor. J. Exp. Zool. 290: 177-181.
2. Akhundov, M.M. 2000. The ecological plasticity of sturgeons sex differentiation. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 267. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.
3. Arai, K. 2001. Genetic improvement of aquaculture finfish species by chromosome manipulation techniques in Japan. Aquaculture 197: 205-228.
4. Baroiller, J.-F. and D'Cotta, H. 2001. Environment and sex determination in farmed fish. Comp. Biochem. Physiol. 130C: 399-409.
5. Baroiller, J.-F., Guiguen, Y. and Fostier, A. 1999. Endocrine and environmental aspects of sex differentiation in fish. Cell. Mol. Life Sci. 55: 910-931.
6. Beardmore, J.A., Mair, G.C. and Lewis, R.I. 2001. Monosex male production in finfish as exemplified by tilapia: Applications, problems, and prospects. Aquaculture 197: 283-301.
7. Chang, C.F., Huang, C.Y., Chiang, M.C. and Lan, S.C. 1999. The concentrations of plasma sex steroids and gonadal aromatase during controlled sex differentiation in grey mullet, Mugil cephalus. Aquaculture 177: 37-45.
8. Chieffi, G. 1957. The reproductive system of elasmobranchs: Development and endocrinological aspects. In: Sharks, Skates and Ray. pp. 553-589. Edited by P.W. Gilbert, R.F. Mathewson and D.P. Rall. John Hopkins Press, Baltimore, Maryland.
9. Colombo, G. and Grandi, G. 1996. Histological study of the development and sex differentiation of the gonad in the European eel. J. Fish Biol. 48: 493-512.
10. Crews, D. 1996. Temperature-dependent sex determination: The interplay of steroid hormones and temperature. Zool. Sci. 13: 1-13.
11. D'Cotta, H., Fostier, A., Guignen, Y., Govoroun, M. and Baroiller, J.-F. 2001. Search for genes involved in the temperature-induced gonadal sex differentiation in the tilapia, Oreochromis niloticus. J. Exp. Zool. 290: 574-585.
12. D'Cotta, H., Guiguen, Y., Govoroun, M., McMeel, O. and Baroiller, J.-F. 2000. Aromatase gene expression in temperature-induced gonadal sex differentiation of tilapia Oreochromis niloticus. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 197-199. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.
13. Devlin, R.H. and Nagahama, Y. 2002. Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences. Aquaculture 208: 191-364.
14. Fedorov, K.E., Zubova, S.E., Semenov, V.V. and Burlakov, A.B. 1990. Secretory cells in the gonads of the young sterlet Acipenser ruthenus during sex differentiation. J. Ichthyol. 30: 65-75.
15. Feist, G., Schreck, C.B., Fitzpatrick, M.S. and Redding, J.M. 1990. Sex steroid profiles of coho salmon (Oncorhynchus kisutch) during early development and sexual differentiation. Gen. Comp. Endocrinol. 80: 299-313.
16. Fitzpatrick, M.S., Pereira, C.B. and Schreck, C.B. 1993. In vitro steroid secretion during early development of mono-sex rainbow trout: Sex differences, onset of pituitary control, and effects of dietary steroid treatment. Gen. Comp. Endocrinol. 91: 199-215.
17. Francis, R.C. 1992. Sexual lability in teleosts: Developmental factors. Quart. Rev. Biol. 67: 1-18.
18. Govoroun, M., McMeel, O.M., D'Cotta, H., Ricordel, M.-J., Smith, T.J., Fostier, A. and Guiguen, Y. 2001a. Steroid enzyme gene expressions during natural and androgen-induced gonadal differentiation in the rainbow trout, Oncorhynchus mykiss. J. Exp. Zool. 290: 558-566.
19. Govoroun, M., McMeel, O.M., Mecherouki, H., Smith, T.J. and Guiguen, Y. 2001b. 17β-estradiol treatment decreases steroidogenic enzyme messenger ribonuclei acid levels in the rainbow trout testis. Endocrinology 142: 1841-1848.
20. Green, B.W. and Teichert-Coddington, D.R. 2000. Human food safety and environmental assessment of the use of 17α-methyltestosterone to produce male tilapia in the United States. J. World Aquaculture Soc. 31: 337-357.
21. Guiguen, Y., Baroiller, J.-F., Ricordel, M.-J., Iseki, K., McMeel, O.M., Martin, S.A.M. and Fostier, A. 1999. Involvement of estrogens in the process of sex differentiation in two fish species: The rainbow trout (Oncorhynchus mykiss) and a tilapia (Oreochromis niloticus). Mol. Reprod. Develop. 54: 154-162.
22. Guiguen, Y., Govoroun, M., D'Cotta, H.D., McMeel, O.M. and Fostier, A. 2000. Steroids and gonadal sex differentiation in the rainbow trout, Oncorhynchus mykiss. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 241-243. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.
23. Hann, H.W. 1927. The history of the germ cells of Cottus bairdie Girard. J. Morphol. Physiol. 43: 427-498.
24. Harder, W. 1975. Anatomy of Fishes. E. Schweizerbart'sche Verlagsbuchhandlung, Stuttgart.
25. Hayes, T.B. 1998. Sex determination and primary sex differentiation in amphibians: Genetic and developmental mechanisms. J. Exp. Zool. 281: 373-399.
26. Hunter, G.A. and Donaldson, E.M. 1983. Hormonal sex control and its application to fish culture. In: Fish Physiology Vol. IX, Part B Behaviour and Fertility Control. pp. 223-303. Edited by W.S. Hoar, J.D. Randall and E.M. Donaldson. Academic Press, New York.
27. Hoar, W.S. 1969 Reproduction. In: Fish Physiology, Vol. III. Reproduction and Growth, Bioluminescence, Pigments, and Poisons. pp. 1-72. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.
28. Hyodo, Y., Tuzuki, E. and Egami, N. 1966. Multiplication of primordial germ cells and initiation of meiosis in the medaka, Oryzias latipes. Japan. J. Exp. Morphol. 20: 98.
29. Ito, L.S., Yamashita, M. and Strüssmann, C.A. 2002. Dynamics of head-induced germ cell loss in pejerrey, Odontesthes bonariensis. Fish. Sci. 68S: in press.
30. Jensen, G.L. and Shelton, W.L. 1983. Gonadal differentiation in relation to sex control of grass carp, Ctenopharyngodon idella (Pisces: Cyprinidae). Copeia 1983: 749-755.
31. Kallman, K.D. 1984. A new look at sex determination in Poeciliid fishes. In: Evolutionary Genetics of Fishes. pp. 95-171. Edited by B.J. Turner. Plenum Press, New York.
32. Kanamori, A., Nagahama, Y. and Egami, N. 1985. Development of the tissue architecture in the gonads of the medaka Oryzias latipes. Zool. Sci. 2: 695-706.
33. Karube, M. 2001. Cloning and expression of cytochrome P450 aromatase and estrogen receptors α and β genes during the critical period of thermolabile sex determination in pejerrey Odontesthes bonariensis. M.Sc. Thesis. Tokyo University of Fisheries, Tokyo, Japan.
34. Kawahara, T. and Yamashita, I. 2000. Estrogen-independent ovary formation in the medaka fish, Oryzias latipes. Zool. Sci. 17: 65-68.
35. Kitano, T., Takamune, K., Kobayashi, T., Nagahama, Y. and Abe, S. 1999. Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus). J. Mol. Endocrinol. 23: 167-176.
36. Kitano, T., Takamune, K., Nagahama, Y. and Abe, S. 2000. Aromatase inhibitor and 17α-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of P450 aromatase gene expression in Japanese flounder (Paralichthys olivaceus). Mol. Reprod. Develop. 56: 1-5.
37. Korpelainen, H. 1990. Sex ratios and conditions required for environmental sex determination in animals. Biol. Rev. 65: 147-184.
38. Kwon, J., Haghpanah, V., Kogson-Hurtado, L.M., McAndrew, B.J. and Penman, D.J. 2000. Masculinization of genetic female Nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J. Exp. Zool. 287: 46-53.
39. Kwon, J., McAndrew, B.J. and Penman, D.J. 2000. Inhibition of aromatase activity suppresses high-temperature feminisation of genetic male Nile tilapia, Oreochromis niloticus. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 268. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.
40. Kurita, M. 1999. Effects of water temperature on the process of gonadal sex differentiation in pejerrey. M.Sc. Thesis. Tokyo University of Fisheries, Tokyo, Japan.
41. Lebrun, C., Billard, R. and Jalabert, B. 1982. Changes in the number of germ cells in the gonads of the rainbow trout (Salmo gairdneri) during the first 10 post-hatching weeks. Reprod. Nutr. Dev. 22: 405-412.
42. 11β. (11β-hydroxylase) gene during gonadal differentiation and spermatogenesis in rainbow trout, Oncorhynchus mykiss. J. Steroid Biochem. Mol. Biol. 75: 291-298.
43. Lofts, B. and Bern, H.B. 1972. The functional morphology of steroidogenic tissue. pp. 37-125. Edited by D.R. Idler. Academic Press, New York.
44. Marchand, O., Govoroun, M., D'Cotta, H.D., McMeel, O.M., Lareyre, J.-J., Bernot, A., Laudet, V. and Guiguen, Y. 2000. DMRT1 expression during gonadal differentiation and spermatogenesis in the rainbow trout, Oncorhynchus mykiss. Biochem. Biophys. Acta 1493: 180-187.
45. Matsuda, M., Nagahama, Y., Shinomiya, A., Satoh, T., Matsuda, C., Kobayashi, T., Morrey, C.E., Shibata, N., Asakawa, S., Shimizu, N., Hori, H., Hamaguchi, S. and Sakaizumi, M. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417: 559-562.
46. Miranda, L.A., Strüssmann, C.A. and Somaza, G.M. 2001. Immunocytochemical identification of GtH1 and GtH2 cells during the temperature-sensitive period for sex determination in pejerrey, Odontesthes bonariensis. Gen. Comp. Endocrinol. 124: 45-52.
47. Nagahama, Y. 2000. Gonadal steroid hormones: Major regulators of gonadal sex differentiation and gametogenesis in fish. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 211-222. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.
48. Nagahama, Y., Kagawa, H. and Young, G. 1982. Cellular sources of sex steroids in teleost gonads. Can. J. Fish. Aquat. Sci. 39: 56-64.
49. Nakamura, M. 1978. Morphological and experimental studies on sex differentiation of the gonad in several teleost fishes. Ph.D. Thesis. Hokkaido University, Hokkaido, Japan.
50. Nakamura, M. 1982. Gonadal sex differentiation in whitespotted char, Salvelinus leucomaenis. Japan. J. Ichthyol. 28: 431-436.
51. Nakamura, M. 1984. Effects of estradiol-17β on gonadal sex differentiation in two species of salmonids, the masu salmon, Oncorhynchus masou, and the chum salmon, O. keta. Aquaculture 43: 83-90.
52. Nakamura, M., Kobayashi, T., Chang, X.-T. and Nagahama, Y. 1998. Gonadal sex differentiation in teleost fish. J. Exp. Zool. 281: 362-372.
53. Nakamura, M., Kobayashi, T., Yoshiura, Y. and Nagahama, Y. 2000. Role of endogenous steroid hormones on gonadal sex differentiation in fish. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 247-249. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Fish Symp 99, Bergen, Norway.
54. Nakamura, M. and Nagahama, Y. 1985. Steroid producing cells during ovarian differentiation of the tilapia Sarotherodon niloticus. Dev. Growth. Differ. 27: 701-708.
55. Nakamura, M. and Nagahama, Y. 1989. Differentiation and development of Leydig cells, and changes of testosterone levels during testicular differentiation in tilapia Oreochromis niloticus. Fish Physiol. Biochem. 7: 211-219.
56. Nakamura, M. and Nagahama, Y. 1993. Ultrastructural study on the differentiation of steroid-producing cells during ovarian differentiation in the amago salmon, Oncorhynchus rhodurus. Aquaculture 112: 237-251.
57. Nakamura, M. and Takahashi, H. 1973. Gonadal sex differentiation in tilapia, with special regard to the time of estrogen treatment effective in inducing complete feminization of genetic males. Bull. Fac. Fish. Hokkaido Univ. 24: 1-13.
58. Nakamura, M., Takahashi, H. and Hiro, O. 1974. Sex differentiation in the masu salmon (Oncorhynchus masou). Sci. Rep. Hokkaido Salmon Hatchery 28: 1-8.
59. Onitake, K. 1972. Morphological studies of normal sex-differentiation and induced sex-reversal process of gonads in the medaka, Oryzias latipes. Annot. Zool. Japan. 45: 159-169.
60. Pandian, T.J. and Koteeswaran, R. 1999. Lability of sex differentiation in fish. Current Science 76: 580-583.
61. Pandian, T.J. and Sheela, S.G. 1995. Hormonal induction of sex reversal in fish. Aquaculture 138: 1-22.
62. Pandian, T.J., Venugopal, T. and Koteeswaran, R. 1999. Problems and prospects of hormone, chromosome and gene manipulations in fish. Current Science 76: 369-386.
63. Parhar, I.S. 1997. GnRH in Tilapia: Three genes, three origins and their roles. In: GnRH Neurons: Gene to Behavior, pp. 99-122. Edited by I.S. Parhar and Y. Sakuma. Brain Shuppan, Tokyo.
64. Patiño, R. 1997. Manipulations of the reproductive system of fishes by means of exogenous chemicals. Prog. Fish-Cult. 59: 118-128.
65. Patiño, R., Davis, K.B., Schoore, J.E., Uguz, C., Strüssmann, C.A., Parker, N.C., Simco, B.A. and Goudie, C.A. 1996. Sex differentiation of channel catfish gonads: Normal development and effects of temperature. J. Exp. Zool. 276: 209-218.
66. Patiño, R. and Takahashi, F. 1995. In: An Atlas of Fish Histology, Normal and Pathological Features (2nd Edition), pp. 128-153. Edited by F. Takashima and T. Hibiya. Kodansha/Gustav Fischer Verlag, Tokyo/Stuttgart.
67. Pieau, C. 1996. Temperature variation and sex determination in reptiles. BioEssays 18: 19-26.
68. Piferrer, F. 2001. Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197: 229-281.
69. Piferrer, F., Zanuy, S., Carrillo, M., Solar, I.I., Devlin, R.H. and Donaldson, E.M. 1994. Brief treatment with an aromatase inhibitor during sex differentiation causes chromosomally female salmon to develop as normal, functional females. J. Exp. Zool. 270: 255-262.
70. Rothbard, S., Moav, B. and Yaron, Z. 1987. Changes in steroid concentrations during sexual ontogenesis in tilapia. Aquaculture 61: 59-74.
71. Satoh, N. 1974. An ultrastructural study of sex differentiation in the teleost Oryzias latipes. J. Embryol. Exp. Morphol. 32: 195-215.
72. Satoh, N. and Egami, N. 1972. Sex differentiation of germ cells in the teleost, Oryzias latipes, during normal embryonic development. J. Embryol. Exp. Morphol. 28: 385-395.
73. Scholz, S. and Gutzeit, H.O. 2000. 17α-ethinylestradiol affects reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes). Aquat. Toxicol. 50: 367-373.
74. Schreck, C.B. 1974. Hormonal treatment and sex manipulation in fishes. In: Control of Sex in Fishes. pp. 84-106. Edited by C.B. Schreck. Virginia Polytechnic Institute and State University, Blacksburg.
75. Schreibman, M.P., Berkowitz, E.J. and Van Den Hurk, R. 1982. Histology and histochemistry of the testis and ovary of the platy-fish, Xiphophorus maculatus, from birth to sexual maturity. Cell Tissue Res. 224: 81-87.
76. Shimizu, M. and Takahashi, H. 1980. Process of sex differentiation of the gonad and gonoduct of the three-spined stickleback, Gasterosteus aculeatus L. Bull. Fac. Fish. Hokkaido Univ. 31: 137-148 (in Japanese).
77. Shinomiya, A., Hamaguchi, S. and Shibata, N. 2001. Sexual differentiation of germ cell deficient gonads in the medaka, Oryzias latipes. J. Exp. Zool. 290: 402-410.
78. Strüssmann, C.A., Karube, M., Miranda, L.A., Patiño, R., Somoza, G.M., Uchida, D. and Yamashita, M. 2002. Methods of sex control in fishes and an overview of novel hypotheses concerning the mechanisms of sex differentiation. In: Fish Genetics and Aquaculture Biotechnology. In press. Edited by T.J. Pandian, C.A. Strüssmann and M.P. Marian. Oxford & IBH Publishing/Science Publishers, New Delhi, India/Enfield, USA.
79. Strüssmann, C.A., Moriyama, S., Hanke, E.F., Calsina Cota, J.C. and Takashima, F. 1996b. Evidence of thermolabile sex determination in pejerrey. J. Fish Biol. 48: 643-651.
80. Strüssmann, C.A. and Patiño, R. 1995. Temperature manipulation of sex differentiation in fish. In: Proceedings of the Fifth International Symposium on the Reproductive Physiology of Fish. pp. 153-160. Edited by F.W. Goertz and P. Thomas. FishSymp95, Austin, Texas.
81. Strüssmann, C.A. and Patiño, R. 1999. Sex determination environmental. In: Encyclopedia of Reproduction. Vol. 4, pp. 402-409. Edited by E. Knobil and J.D. Neill. Academic Press.
82. Strüssmann, C.A., Saito, T., Usui, M., Yamada, H. and Takashima, F. 1997. Thermal thresholds and critical period of thermolabile sex determination in two atherinid fishes, Odontesthes bonariensis and Patagonina hatcheri. J. Exp. Zool. 278: 167-177.
83. Strüssmann, C.A., Takashima, F. and Toda, K. 1996a. Sex differentiation and hormonal feminisation in pejerrey Odontesthes bonariensis. Aquaculture 139: 31-45.
84. Sumpter, J.P. 1997. Environmental control of fish reproduction: A different perspective. Fish Physiol. Biochem. 17: 25-31.
85. Takahashi, H. 1977. Juvenile hermaphroditism in the zebrafish, Brachydanio rerio. Bull. Fac. Fish. Hokkaido Univ. 28: 57-65.
86. Takahashi, H. and Iwasaki, Y. 1973. The occurrence of histochemical activity of 3β-hydroxysteroid dehydrogenase in the developing testes of Poecilia reticulata. Dev. Growth Differ. 15: 241-253.
87. Takahashi, H. and Shimizu, M. 1983. Juvenile intersexuality in a cyprinid fish, the Sumatra barb, Barbus tetrazona tetraxona. Bull. Fac. Fish. Hokkaido Univ. 34: 69-78.
88. Thorgaard, G.H. 1983. Chromosome set manipulation and sex control in fish. In: Fish Physiology, Vol. IX, Part B, Behavior and Fertility Control. pp. 405-434. Edited by W.S. Hoar, D.J. Randall and E.M. Donaldson. Academic Press, New York.
89. Trant, J.M., Gavasso, S., Ackers, J., Chung, B.-C. and Place, A.R. 2001. Developmental expression of cytochrome P450 aromatase genes (CYP19a and CYP19b) in zebrafish fry (Danio rerio). J. Exp. Zool. 290: 475-483.
90. Tuzuki, E., Egami, N. and Hyodo, Y. 1966. Multiplication and sex differentiation of germ cells during development in the medaka, Oryzias latipes. Japan. J. Ichthyol. 13: 176-182.
91. Uchida, D., Yamashita, M., Kitano, T. and Iguchi, T. 2002. Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J. Exp. Biol. 205: 711-718.
92. Van Den Hurk, R. 1974. Steroidogenesis in the testis and gonadotropic activity in the pituitary during postnatal development of the black molly (Mollienesia latipinna). Proc. Kon. Ned. Akad. Wet. C77: 193-200.
93. Van Den Hurk, R., Lambert, J.G.D. and Peute, J. 1982. Steroidogenesis in the gonads of rainbow trout fry (Salmo gairdneri) before and after the onset of gonadal sex differentiation. Reprod. Nutr. Dev. 22: 413-425.
94. Witschi, E. 1957. The inductor theory of sex differentiation. J. Fac. Hokkaido Univ. Ser. VI Zool. 13: 428-439.
95. Yamamoto, T. 1953. Artificially induced sex reversal in genotypic males of the medaka (Oryzias latipes). J. Exp. Zool. 123: 571-594.
96. Yamamoto, T. 1969. Sex differentiation. In: Fish Physiology Vol. III, Reproduction and Growth, Bioluminescence, Pigments, and Poisons. pp. 117-175. Edited by W.S. Hoar and D.J. Randall. Academic Press, New York.
97. Yamazaki, F. 1983. Sex control and manipulation of fish. Aquaculture 33: 329-354.
98. Yoshikawa, H. and Oguri, M. 1978. Gonadal sex differentiation in the medaka, Oryzias latipes, with special regard to the gradient of the differentiation of testes. Bull. Japan. Fish. Sci. Soc. 45: 1115-1121.
99. Yoshizaka, G., Takeuchi, Y., Kobayashi, T., Ihara, S. and Takeuchi, T. 2002. Primordial germ cells: The blueprint for a piscine life. Fish Physiol. Biochem. 26: 3-12.
100. Zanuy, S., Carrillo, M., Felip, A., Rodríguez, L., Blázquez, M., Ramos, J. and Piferrer, F. 2001. Genetic, hormonal and environmental approaches for the control of reproduction in the European sea bass (Dicentrarchus labrax L.). Aquaculture 202: 187-203.