Hormonal and pheromonal control of spawning behavior in the goldfish

Fish Physiology and Biochemistry

Volumn 26, Issue 1, 2002, Pages 71-84

  Kobayashi, Makito ^a   Sorensen, Peter W ^b   Stacey, Norm E ^c  

^a INTERNATIONAL CHRISTIAN UNIVERSITY   (Japan)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

11 KETOANDROSTENDIONE; 11 OXOTESTOSTERONE; 15 OXOPROSTAGLANDIN F2 ALPHA; 17,20BETA DIHYDROXYPREGN 4 EN 3 ONE; ANDROGEN; ANDROSTENEDIONE; ESTRADIOL; GESTAGEN; GONADORELIN; LUTEINIZING HORMONE; PHEROMONE; PROSTAGLANDIN F2 ALPHA; SEX HORMONE; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL REPRODUCTIVE PROCEDURES; ENVIRONMENTAL FACTOR; ENVIRONMENTAL TEMPERATURE; FERTILIZER APPLICATION; GAMETE; GENITAL SYSTEM; GOLDFISH; GONAD; HORMONAL REGULATION; HORMONE BLOOD LEVEL; HORMONE RELEASE; HORMONE SYNTHESIS; NONHUMAN; OOCYTE MATURATION; OVIDUCT; OVULATION; REVIEW; SEXUAL BEHAVIOR; SEXUAL MATURATION; SPAWNING; SPERMATOGENESIS; STEROIDOGENESIS; TELEOST; TESTOSTERONE BLOOD LEVEL; VITELLOGENESIS;

ANIMALIA; CARASSIUS AURATUS; PISCES; TELEOSTEI;

EID: 0038075444     PISSN: 09201742     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1023375931734     Document Type: Review

References (106)

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. Muller-Schwarze and P.W. Sorensen. Kluwer Academic/Plenum Publishers, New York.
2. Barry, T.P., Santos, A.T.G., Furukawa, K., Aida, K. and Hanyu, I. 1990. Steroid profiles during spawning in male common carp. Gen. Comp. Endocrinol. 80: 223-231.
3. Bayley, M., Nielsen, J.R. and Baatrup, E. 1999. Guppy sexual behavior as an effect biomarker of estrogen mimics. Ecotoxicol. Environ. Safety 43: 68-73.
4. Bjerselius, R., Olsen, K.H. and Zheng, W. 1995. Endocrine, gonadal and behavioral responses of male crucian carp to the hormonal pheromone 17α,20β-dihydroxy-4-pregnen-3-one. Chem. Senses 20: 221-230.
5. Bjerselius, R., Lundstedt-Enkel, K., Olsen, H., Mayer, I. and Dimberg, K. 2001. Male goldfish reproductive behavior and physiology are severely affected by exogenous exposure to 17β-estradiol. Aquatic Toxicol. 52: 139-152.
6. Blaustein, J.D. and Erskine, M.S. 2002. Feminine sexual behavior: Cellular integration of hormonal and afferent information in the rodent brain. In: Hormones, Brain and Behavior. pp. 139-214. Edited by D.W. Pfaff, A.P. Arnold, A. Etgen, S. Fahrbach and R. Rubin. Academic Press, New York.
7. Borg, B. 1994. Androgens in teleost fishes. Comp. Biochem. Physiol. 109C: 219-245.
8. Cardwell, J.R., Stacey, N.E., Tan, E.S.P., McAdam, D.S.O. and Lang, S.L.C. 1995. Androgen increases olfactory receptor response to a vertebrate sex pheromone. J. Comp. Physiol. A 176: 55-61.
9. Chang, J.P. and Peter, R.E. 1983. Effects of dopamine on gonadotropin release in female goldfish, Carassius auratus. Neuroendocrinology 36: 351-357.
10. Cheek, A.O., Thomas, P. and Sullivan, C.V. 2000. Sex steroids relative to alternative mating behaviors in the simultaneous hermaphrodite Serranus subligarius (Perciformes: Serranidae). Horm. Behav. 37: 198-211.
11. Cole, K.S. and Stacey, N.E. 1984. Prostaglandin induction of spawning behavior in Cichlasoma bimaculatum (Pisces Cichlidae). Horm. Behav. 18: 235-248.
12. Colombo, L., Belvedere, P.C., Marconato, A. and Bentivegna, F. 1982. Endocrinology of teleost reproduction. In: Proceedings of the Second International Symposium on the Reproductive Physiology of Fish. pp. 84-94. Edited by C.J.J. Richter and H.J.Th. Goos Pudoc, The Netherlands.
13. DeFraipont, M. and Sorensen, P.W. 1993. Exposure to the pheromone 17α, 20β-dihydroxy-4-pregnen-3-one enhances the behavioral spawning success, sperm production, and sperm motility of male goldfish. Anim. Behav. 46: 245-256.
14. Dulka, J.G., Sorensen, P.W. and Stacey, N.E. 1987a. Socially-stimulated gonadotropin release in male goldfish: Differential circadian sensitivities to a steroid pheromone and spawning stimuli. In: Proceedings of the Third International Symposium on the Reproductive Physiology of Fish. p. 160. Edited by D.R. Idler, L.W. Crim and J.M. Walsh. Memorial University Press, St. John's, Newfoundland.
15. Dulka, J.G., Stacey, N.E., Sorensen, P.W. and Van Der Kraak, G.J. 1987b. A sex steroid pheromone synchronizes male-female spawning readiness in goldfish. Nature 325: 251-253.
16. Dulka, J.G., Sloley, B.D., Stacey, N.E. and Peter, R.E. 1992. A reduction in pituitary dopamine turnover is associated with sex pheromone-induced gonadotropin increase in goldfish. Gen. Comp. Endocrinol. 86: 496-505.
17. Elofsson, U., Winberg, S. and Francis, R.C. 1997. Number of pre-optic GnRH-immunoreactive cells correlates with sexual phase in a protandrously hermaphroditic fish, the dusky anemone fish (Amphiprion melanopus). J. Comp. Physiol. A 181: 484-492.
18. Elofsson, U., Winberg, S. and Nilsson, G.E. 1999. Relationships between sex and the size and number of forebrain gonadotropin-releasing hormone-immunoreactive neurons in the ballan wrasse (Labrus berggylta), a protogynous hermaphrodite. J. Comp. Neurol. 410: 158-170.
19. Fraser, E.J. and Stacey, N.E. 2002. Isolation increases milt production in goldfish. J. Exp. Zool. 293: 511-524.
20. Godwin, J., Crews, D. and Warner, R.R. 1996. Behavioural sex change in the absence of gonads in a coral reef fish. Proc. Roy. Soc. Lond. B. 263: 1683-1688.
21. Godwin, J., Sawby, R., Warner, R.R., Crews, D. and Grober, M.S. 2000. Hypothalamic arginine vasotocin mRNA abundance variation across sexes and with sex change in a coral reef fish. Brain Behav. Evol. 55: 77-84.
22. Grober, M.S., and Sunobe, T. 1996. Serial adult sex change involves rapid and reversible changes in brain neuro-chemistry. Neuroreport 7: 2945-2949.
23. Grober, M.S., Jackson, I.M.D. and Bass, A.H. 1991. Gonadal steroids affect LHRH preoptic cell number in a sex/role changing fish. J. Neurobiol. 22: 734-741.
24. Howell, W.M., Black, D.A. and Bortone, S.A. 1980. Abnormal expression of secondary sex characters in a population of mosquitofish, Gambusia affinis holbrooki: Evidence for environmentally-induced masculinization. Copeia 1980: 676-681.
25. Irvine, I.A.S. and Sorensen, P.W. 1993. Acute olfactory sensitivity of wild common carp, Cyprinus carpio, to goldfish sex pheromones is influenced by gonadal maturity. Can. J. Zool. 71: 2199-2210.
26. Kagawa, H., Young, G. and Nagahama, Y. 1984. In vitro 17β-estradiol and testosterone production by ovarian follicles of the goldfish, Carassius auratus. Gen. Comp. Endocrinol. 54: 139-143.
27. Kalra, S.P. and Kalra, P.S. 1997. Interactive hypothalamic neural circuitry in the control of reproduction: A bird's eye view. In: Neural Control of Reproduction. pp. 3-16. Edited by K.-I. Maeda, H. Tsukamura and A. Yokoyama. Japan Sci. Soc. Press, Tokyo.
28. Kezuka, H., Kobayashi, M., Aida, K. and Hanyu, I. 1989. Effects of photoperiod and pinealectomy on the gonadotropin surge and ovulation in goldfish Carassius auratus. Nippon Suisan Gakkaishi 55: 2099-2103.
29. Kim, M.H., Oka, Y., Amano, M., Kobayashi, M., Okuzawa, K., Hasegawa, Y., Kawashima, S., Suzuki, Y. and Aida, K. 1995. Immunohistochemical localization of sGnRH and cGnRH-II in the brain of goldfish, Carassius auratus. J. Comp. Neurol. 356: 72-82.
30. Kim, M.H., Kobayashi, M., Oka, Y., Amano, M., Kawashima, S. and Aida, K. 2001. Effects of olfactory tract section on the immunohistochemical distribution of the brain GnRH fibers in the female goldfish, Carassius auratus. Zool. Sci. 18: 241-248.
31. Kime, D.E. 1998. Endocrine Disruption in Fish. Kluwer Academic Publishers, Boston.
32. Kindler, P.M., Bahr, J.M. and Philipp, D.P. 1991. The effects of exogenous 11-ketotestosterone, testosterone, and crypterone acetate on prespawning and parental care behaviors of male bluegill. Horm. Behav. 25: 410-423.
33. Kitamura, S., Ogata, H. and Takashima, F. 1994. Activities of F-type prostaglandins as releaser sex pheromones in cobitide loach, Misgurnus anguillicaudatus. Comp. Biochem. Physiol. 107A: 161-169.
34. Kobayashi, M. and Stacey, N. E. 1993. Prostaglandin-induced female spawning behavior in goldfish (Carassius auratus) appears independent of ovarian influence. Horm. Behav. 27: 38-55.
35. Kobayashi, M. and Nakanishi, T. 1999. 11-Ketotestosterone induces male-type sexual behavior and gonadotropin secretion in gynogenetic crucian carp, Carassius auratus langsdorfii. Gen. Comp. Endocrinol. 115: 178-187.
36. Kobayashi, M., Aida, K. and Hanyu, I. 1986a. Gonadotropin surge during spawning in male goldfish. Gen. Comp. Endocrinol. 62: 70-79.
37. Kobayashi, M., Aida, K. and Hanyu, I. 1986b. Pheromone from ovulatory female goldfish induces gonadotropin surge in males. Gen. Comp. Endocrinol. 63: 451-455.
38. Kobayashi, M., Aida, K. and Hanyu, I. 1986c. Annual changes in plasma levels of gonadotropin and steroid hormones in goldfish. Bull. Japan. Soc. Sci. Fish. 52: 1153-1158.
39. Kobayashi, M., Aida, K. and Hanyu, I. 1987. Hormone changes during ovulation and effects of steroid hormones on plasma gonadotropin levels and ovulation in goldfish. Gen. Comp. Endocrinol. 67: 24-32.
40. Kobayashi, M., Aida, K. and Hanyu, I. 1988. Hormone changes during the ovulatory cycle in goldfish. Gen. Comp. Endocrinol. 69: 301-307.
41. Kobayashi, M., Aida, K. and Hanyu, I. 1989a. Involvement of steroid hormones in the preovulatory gonadotropin surge in female goldfish. Fish Physiol. Biochem. 7: 141-146.
42. Kobayashi, M., Aida, K. and Hanyu, I. 1989b. Induction of gonadotropin surge by steroid hormone implantation in ovariectomized and sexually regressed female goldfish. Gen. Comp. Endocrinol. 73: 469-476.
43. Kobayashi, M., Aida, K. and Stacey, N.E. 1991. Induction of testis development by implantation of 11-ketotestosterone in female goldfish. Zool. Sci. 8: 389-393.
44. Kobayashi, M., Amano, M., Kim, M. H., Furukawa, K., Hasegawa, Y. and Aida, K. 1994. Gonadotropin-releasing hormones of terminal nerve origin are not essential to ovarian development and ovulation in goldfish. Gen. Comp. Endocrinol. 95: 192-200.
45. Kobayashi, M., Furukawa, K., Kim, M. H. and Aida, K. 1997. Induction of male-type gonadotropin secretion by implantation of 11-ketotestosterone in female goldfish. Gen. Comp. Endocrinol. 108: 434-445.
46. Kobayashi, M., Stacey, N.E., Aida, K. and Watabe, S. 2000. Sexual plasticity of behavior and gonadotropin secretion in goldfish and gynogenetic crucian carp. In: Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. pp. 117-125. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Institute of Marine Research and University of Bergen, Bergen.
47. Landsman, R.E., David, L.A. and Drew, B. 1987. Effects of 17α-methyltestosterone and mate size on sexual behavior in Poecilia reticulata. In: Proceedings of the Third International Symposium on the Reproductive Physiology of Fish. p. 133. Edited by D.R. Idler, L.W. Crim and J.M. Walsh. Memorial University of Newfoundland, St. John's.
48. Liley, N.R. 1972. The effects of estrogens and other steroids on the sexual behavior of the female guppy, Poecilia reticulata. Gen. Comp. Endocrinol. Suppl. 3: 542-552
49. Liley, N.R. and Stacey, N.E. 1983. Hormones, pheromones and reproductive behaviour. In: Fish Physiology. Volume 9B. pp. 1-63. Edited by W.S. Hoar, D.J. Randall, and E.M. Donaldson. Academic Press, New York.
50. Liley, N.R. and Tan, E.S.P. 1985. The induction of spawning behavior in Puntius gonionotus (Bleeker) by treatment with prostaglandin PGF2α. J. Fish Biol. 26: 491-502.
51. Liley, N.R. and Kroon, F.J. 1995. Male dominance, plasma hormone concentrations, and availability of milt in male rainbow trout (Oncorhynchus mykiss). Can. J. Zool. 73: 826-836.
52. Murphy, C.A. and Stacey, N.E. 2002. Methyl-testosterone induces male-typical ventilatory behavior in response to putative steroidal pheromones in female round gobies (Neogobius melanostomus). Horm. Behav. 42: 109-115.
53. Murphy, C.A., Stacey, N. and Corkum, L.D. 2001. Putative steroidal pheromones in the round goby, Neogobius melanostomus: Olfactory and behavioral responses. J. Chem. Ecol. 27: 443-470.
54. Nakashima, Y., Sakai, Y., Karino, K. and Kuwamura, T. 2000. Female-female spawning and sex change in a haremic coral-reef fish, Labroides dimidiatus. Zool. Sci. 17: 967-970.
55. Oshima, Y., Kang, I.J., Kobayashi, M., Nakayama, K., Imada, N. and Honjo, T. 2002. Suppression of sexual behavior in male Japanese medaka (Oryzias latipes) exposed to 17β-estradiol. Chemosphere 50: 429-436.
56. Parhar, I., Tosaki, H., Sakuma, Y. and Kobayashi, M. 2001. Sex differences in the brain of goldfish: Gonadotropin-releasing hormones and vasotocinergic neurons. Neurosci. 104: 1099-1110.
57. Patiño, R., Yoshizaki, G., Thomas, P. and Kagawa, H. 2001. Gonadotropic control of ovarian follicle maturation: The two-stage concept and mechanisms. Comp. Biochem. Physiol. B. 129: 427-439.
58. Pfaff, D.W., Arnold, A.P., Etgen, A., Fahrbach, S. and Rubin, R. 2002a. Series Editors. Hormones, Brain and Behavior, Volume 2. Academic Press, New York.
59. Pfaff, D.W., Arnold, A.P., Etgen, A., Fahrbach, S. and Rubin, R. 2002b. Series Editors. Hormones, Brain and Behavior, Volume 4. Academic Press, New York.
60. 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.
61. Santos, A.J.G., Furukawa, K., Kobayashi, M., Bando, K., Aida, K. and Hanyu, I. 1986. Plasma gonadotropin and steroid hormone profiles during ovulation in the carp Cyprinus carpio. Bull. Japan. Soc. Sci. Fish. 52: 1159-1166.
62. Schoenfuss, H.L., Levitt, J.T., Van Der Kraak, G. and Sorensen, P.W. 2002. Ten week exposure to treated sewage discharge has relatively minor, variable effects on reproductive behavior and sperm production in goldfish. Environ. Toxicol. Chem. 21: 2185-2190.
63. Scott, A.P. and Sorensen, P.W. 1994. Time course of release of pheromonally active steroids and their conjugates by ovulatory goldfish. Gen. Comp. Endocrinol. 96: 309-323.
64. Sokolowska, M., Peter, R.E., Nahorniak, C.S., Pan, C.H., Chang, J.P., Crim, L.W. and Weil, C. 1984. Induction of ovulation in goldfish, Carassius auratus, by pimozide and analogues of LH-RH. Aquaculture 36: 71-83.
65. Sorensen, P.W. and Stacey, N.E. 1987. 17α,20β-dihdroxy-4-pregnen-3-one functions as a bisexual priming pherome in goldfish. Am. Zool. 27: 412.
66. Sorensen, P.W. and Goetz, F.W. 1993. Pheromonal and reproductive function of F-prostaglandins and their metabolites in teleost fish. J. Lipid Mediators 6: 385-393.
67. Sorensen, P.W. and Scott, A.P. 1994. The evolution of hormonal sex pheromones in teleost fish: Poor correlation between the pattern of steroid release by goldfish and olfactory sensitivity suggests that these cues evolved as a result of chemical spying rather than signal specialization. Acta Scand. Physiol. 152: 191-205.
68. Sorensen, P.W. and Stacey, N.E. 1999. Evolution and specialization of fish hormonal pheromones. In: Advances in Chemical Signals in Vertebrates. pp. 15-47. Edited by R.E. Johnston, D.Muller-Schwarze and P.W. Sorensen. Kluwer Academic/Plenum Publishers, New York.
69. Sorensen, P.W., Hara, T.J. and Stacey, N.E. 1987. Extreme olfactory 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.
70. Sorensen, P.W., Stacey, N.E. and Chamberlain, K.J. 1989. Differing behavioral and endocrinological effects of two female sex pheromones on male goldfish. Horm. Behav. 23: 317-332.
71. Sorensen, P.W., Christensen, T.A. and Stacey, N.E. 1998. Discrimination of pheromonal cues in fish: Emerging parallels with insects. Curr. Opin. Neurobiol. 8: 458-467.
72. 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 Sixth International Symposium on the Reproductive Physiology of Fish. pp. 125-128. Edited by B. Norberg, O.S. Kjesbu, G.L. Taranger, E. Andersson and S.O. Stefansson. Institute of Marine Research and University of Bergen, Bergen.
73. Sorensen, P.W., Hara, T.J., Stacey, N.E. and Goetz, F.W. 1988. F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 39: 1039-1050.
74. Sorensen, P.W., Hara, T.J., Stacey, N.E. and Dulka, J.G. 1990. Extreme olfactory specificity of the male goldfish to the preovulatory steroidal pheromone 17α,20β-dihydroxy-4-pregnen-3-one. J. Comp. Physiol. A. 166: 373-383.
75. Sorensen, P.W., Scott, A.P., Stacey, N.E. and Bowdin, L. 1995a. Sulfated 17α,20β-dihydroxy-4-pregnen-3-one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. General and Comparative Endocrinology 100: 128-142.
76. Sorensen, P.W., Brash, A.R., Goetz, F.W., Kellner, R.G., Bowdin, L. and Vrieze, L.A. 1995b. Origins and functions of F prostaglandins as hormones and pheromones in the goldfish. In: Proceedings of the Fourth International Symposium on the Reproductive Physiology of Fish. pp. 252-254. Edited by F.W. Goetz and P. Thomas. FishSymp 95, Austin, Texas, U.S.A.
77. Stacey, N.E. 1976. Effects of indomethacin and prostaglandins on the spawning behavior of female goldfish. Prostaglandins 12: 113-126.
78. Stacey, 1987. Roles of hormones and pheromones in fish reproductive behavior. In: Psychobiology of Reproductive Behavior, an Evolutionary Perspective. pp. 28-60. Edited by D. Crews. Prentice-Hall, Englewood Cliffs, NJ, U.S.A.
79. Stacey, N.E. 1991. Hormonal pheromones in fish: Status and prospects. In: Proceedings of the Fourth International Symposium on the Reproductive Physiology of Fish. pp. 177-181. Edited by A.P. Scott, J.P. Sumpter, D.S. Kime and M.S. Rolfe. FishSymp 91, Sheffield.
80. Stacey, N.E. and Liley, N.R. 1974. Regulation of spawning behavior in the female goldfish. Nature 247: 71-72.
81. Stacey, N.E. and Peter, R.E. 1979. Central action of prostaglandins in spawning behavior of female goldfish. Physiol. Behav. 22: 1191-1196.
82. Stacey, N.E. and Kyle, A.L. 1983. Effects of olfactory tract lesions on sexual and feeding behavior in the goldfish. Physiol. Behav. 30: 621-628.
83. Stacey, N.E. and Kobayashi, M. 1996. Androgen induction of male sexual behaviors in female goldfish. Horm. Behav. 30: 434-445.
84. Stacey, N.E. and Sorensen, P.W. 2002. Fish hormonal pheromones. In: Hormones, Brain, and Behavior. Volume 2. pp. 375-435. Edited by D.W. Pfaff, A.P. Arnold, A. Etgen, S. Fahrbach and R. Rubin. Academic Press, New York.
85. Stacey, N.E., Cook, A.F. and Peter, R.E. 1979a. Ovulatory surge of gonadotropin in the goldfish Carassius auratus. Gen. Comp. Endocrinol. 37: 246-249.
86. Stacey, N.E., Cook, A.F. and Peter, R.E. 1979b. Spontaneous and gonadotropin induced ovulation in the goldfish, Carassius auratus. L.: Effects of external factors. J. Fish Biol. 15: 305-316.
87. Stacey, N.E., Zheng, WB. and Cardwell, J.R. 1994. Milt production in common carp (Cyprinus carpio): Stimulation by a goldfish steroid pheromone. Aquaculture 127: 265-276.
88. 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. Endocr. 75: 62-70.
89. Stacey, N.E., Fraser, E.J., Sorensen, P.W. and Der Kraak, G.J. 2001. Milt production in goldfish: Regulation by multiple social stimuli. Comp. Biochem. Physiol. C 130: 467-476.
90. Stacey, N.E., Chojnacki, A., Narayanan, A., Cole, TB. and Murphy, C.A. Hormonally-derived sex pheromones in fish: Exogenous cues and signals from gonad to brain. Can. J. Physiol. Pharmacol. (in press).
91. Strüssmann, C.A. and Nakamura, M. 2003. Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes. Fish Physiol. Biochem., in press.
92. Taylor, J. and Mahon, R. 1977. Hybridization of Cyprinus carpio and Carassius auratus, the first two exotic species in the lower Laurentian Great Lakes. Environ. Biol. Fishes1: 205-208.
93. Trudeau, V.L., Wade, W.G., Van Der Kraak, G. and Peter, R.E. 1993. Effects of 17β-estradiol on pituitary and testicular function in male goldfish. Can J. Zool.71: 1131-1135.
94. Van Der Kraak, G., Chang, J.P. and Janz, D.M. 1998. Reproduction. In: The Physiology of Fishes, Second Edition. pp. 465-488. Edited by D.H. Evans. CRC Press, New York.
95. Villars, T.R. and Burdick, M. 1986. Rapid decline in the behavioral response of paradise fish (Macropodes opercularis) to prostaglandin F2α treatment. Gen. Comp. Endocrinol. 63: 157-161.
96. Volkoff, H. and Peter, R.E. 1999. Actions of two forms of gonadotropin releasing hormone and a GnRH antagonist on spawning behavior of the goldfish Carassius auratus. Gen. Comp. Endocrinol. 116: 347-355.
97. Wai, E.H. and Hoar, W.S. 1963. The secondary sex characters and reproductive behavior of gonadectomized sticklebacks treated with methyl testosterone. Can. J. Zool. 41: 611-628.
98. Yamamoto, N., Oka, Y. and Kawashima, S. 1997. Lesions of gonadotropin-releasing hormone-immunoreactive terminal nerve cells: Effects on the reproductive behavior of male dwarf gouramis. Neuroendocrinol. 65: 403-412.
99. Yamanouchi, K. 1997. Brain mechanisms inhibiting the expression of heterotypical sexual behavior in rats. In: Neural Control of Reproduction. pp. 291-235. Edited by K.-I. Maeda, H. Tsukamura and A. Yokoyama. Japan Sci. Soc. Press, Tokyo.
100. Yamazaki, F. 1965. Endocrinological studies on the reproduction of the female goldfish, Carassius auratus L., with special reference to the function of the pituitary gland. Mem. Fac. Fisher. Hokkaido Univ. 13: 1-64.
101. Yamazaki, F. 1990. The role of urine in sex discrimination in the goldfish Carassius auratus. Bull. Fac. Fish. Hokkaido Univ. 41: 155-161.
102. Yamazaki, F. and Watanabe, K. 1979. The role of sex hormones in sex recognition during spawning behavior of the goldfish, Carassius auratus. L. Proc. Indian Natl. Sci. Acad. Part B 45: 505-511.
103. Yoshiura, Y., Kobayashi, M., Kato, Y. and Aida, K. 1997. Molecular cloning of the cDNAs encoding two gonadotropin β subunits (GTH Iβ and IIβ) from the goldfish. Gen. Comp. Endocrinol. 105: 379-389.
104. Zheng, W. and Stacey, N.E. 1996. Two mechanisms for increasing milt volume in male goldfish. J. Exp. Zool. 276: 287-295.
105. Zheng, W. and Stacey, N.E. 1997. A steroidal pheromone and spawning stimuli act via different neuroendocrine mechanisms to increase gonadotropin and milt volume in male goldfish (Carassius auratus). Gen. Comp. Endocrinol. 105: 228-235.
106. Zheng, W., Strobeck, C. and Stacey, N.E. 1997. The steroid pheromone 4-pregnen-17α,20β-diol-3-one increases fertility and paternity in goldfish. J. Exp. Biol. 200: 2833-2840.