Skip to main content
SpringerLink
Log in

Annual reproductive cycle of the captive female Japanese sardineSardinops melanostictus: Relationship to ovarian development and serum levels of gonadal steroid hormones

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Gonad and blood samples were taken from the captive female Japanese sardineSardinops melanostictus between 1988 and 1989, and changes in serum levels of gonadal steroids were correlated with the annual gonadal cycle. Under captive conditions, female fish did not mature and spawn spontaneously, although oocytes developed up to the end of vitellogenic growth. Based on evidence from ovarian histology, the annual gonadal cycle of the Japanese sardine was divisible into four periods, i.e., immature (June to October), vitellogenesis (November to December), spawning (January to March), and post-spawning (April to May). The pattern of seasonal change in the gonadosomatic index (GSI) showed an inverse correlation to change in water temperature and reflected the degree of ovarian maturity. The serum estradiol-17β level increased from its lowest concentration (0.12 ng ml−1) in September to a peak (1.14 ng ml−1) in March. Serum 17α,20β-dihydroxy-4-pregnen-3-one (17α,20β-P) was detectable at low levels (<0.3 ng ml−1) between October and February, but was below the assay detection limit (0.06 ng ml−1) at all other times. Testosterone was not detectable (<0.06 ng ml−1) in the serum of any fish throughout the year. The effects of several steroids on the maturation of follicle-enclosed oocytes of sardine were examined in vitro, and 17α,20β-P was found to be the most potent inducer of maturation. This suggests that post-vitellogenic oocytes of the Japanese sardine in captivity have an ability to respond to an appropriate hormonal effector and subsequently to resume meiotic maturation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Asami, T. (1953). Studies on the ovarian eggs of clupeoid fishes. Bull. Jap. Soc. scient. Fish. 19: 398–404 (in Japanese with English summary)

    Google Scholar 

  • Burke, M. G., Leatherland, J. F., Sumpter, J. P. (1984). Seasonal changes in serum testosterone, 11-ketotestosterone, and 17β-estradiol levels in the brown bullhead,Ictalurus nebulosus Lesueur. Can. J. Zool. 62: 1195–1199

    Google Scholar 

  • Campbell, C. M.., Walsh, J. M., Idler, D. R. (1976). Steroids in the plasma of the winter flounder (Pseudopleuronectes americanus Walbaum): a seasonal study and investigation of steroid involvement in oocyte maturation. Gen. comp. Endocr. 29: 14–20

    Google Scholar 

  • Crim, L. W., Idler, D. R. (1978). Plasma gonadotrophin, estradiol, and vitellogenin and gonad phosvitin levels in relation to the seasonal reproductive cycles of female brown trout. Annls Biol. anim. Biochim. Biophys. 18: 1001–1005

    Google Scholar 

  • De Vlaming, V., Fitzgerald, R., Delahunty, G., Cech, J. J., Selman K., Barkley, M. (1984). Dynamics of oocyte development and related changes in serum estradiol 17-β, yolk precursor and lipid levels in the teleostean fishLeptocottus armatus. Comp. Biochem. Physiol. 77A: 599–610

    Google Scholar 

  • Dindo, J. J., MacGregor, R. (1981). Annual cycle of serum gonadal steroids and serum lipids in striped mullet. Trans. Am. Fish. Soc. 110: 403–409

    Google Scholar 

  • Donaldson, E. M., Hunter, G. A. (1983). Induced final maturation, ovulation, and spermiation in cultured fish. In: Hoar, W. S., Randall, D. J., Donaldson, E. M. (eds.) Fish physiology, Vol. IXB. Academic Press, New York, p. 351–403

    Google Scholar 

  • Dye, H. M., Sumpter, J. P., Fagerlund, U. H. M., Donaldson, E. M. (1986). Changes in reproductive parameters during the spawning migration of pink salmon,Oncorhynchus gorbuscha (Walbaum). J. Fish Biol. 29: 167–176

    Google Scholar 

  • Fitzpatrich, M. S., Van Der Kraak, G., Schreck, C. B. (1986). Profiles of plasma sex steroids and gonadotropin in coho salmon,Oncorhynchus kisutch, during final maturation. Gen. comp. Endocr. 62: 437–451

    Google Scholar 

  • Goetz, F. W. (1983). Hormonal control of oocyte final maturation and ovulation in fishes. In: Hoar, W. S., Randall, D. J., Donaldson, E. M. (eds.) Fish physiology, Vol. IXB. Academic Press, New York, p. 117–170

    Google Scholar 

  • Goetz, F. W., Bergman, H. L. (1978). The effects of steroids on final maturation and ovulation of oocytes from brook trout (Salvelinus fontinalis) and yellow perch (Perca flavescens). Biol. Reprod. 18: 293–298

    Google Scholar 

  • Hiramoto, K. (1973). Studies on the life of the Japanese sardine,Sardinops melanosticta (Temminck et Schlegel), off the Boso Peninsula and in Tokyo Bay, central Japan — I. Aggregation of immatures and adults, and maturation of I-aged fish. Jap. J. Ecol. 23: 110–125 (in Japanese with English summary)

    Google Scholar 

  • Hirose, K., Adachi, S., Nagahama, Y. (1985). Changes in plasma steroid hormone levels during sexual maturation in the ayuPlecoglossus altivelis. Bull. Jap. Soc. scient. Fish. 51: 398–403

    Google Scholar 

  • Ishida, R., Ukawa, M., Arita, S. (1959). On the number of spawning times of sardineSardinops melanosticta (Temminck and Schlegel). Bull. Hokkaido reg. Fish. Res. Lab. 20: 139–146 (in Japanese with English summary)

    Google Scholar 

  • Ito, S. (1961). Fishery biology of the sardine,Sardinops melanosticta (T. & S), in the waters around Japan. Bull. Japan Sea reg. Fish. Res. Lab. 9: 1–227 (in Japanese)

    Google Scholar 

  • Kagawa, H., Takano, K., Nagahama, Y. (1981). Correlation of plasma estradiol-17β and progesterone levels with ultrastructure and histochemistry of ovarian follicles in the white-spotted char,Salvelinus leucomaenis. Cell Tissue Res. 218: 315–329

    Google Scholar 

  • Kagawa, H., Young, G., Adachi, S., Nagahama, Y. (1982). Estradiol-17β production in amago salmon (Oncorhynchus rhodurus) ovarian follicles: role of the thecal layer and granulosa cells. Gen. comp. Endocr. 47: 440–448

    Google Scholar 

  • Kagawa, H., Young, G., Nagahama, Y. (1983a). Relationships between seasonal plasma estradiol-17β and testosterone levels in vitro production by ovarian follicles of amago salmon (Oncorhynchus rhodurus). Biol. Reprod. 29: 301–309

    Google Scholar 

  • Kagawa, H., Young, G., Nagahama, Y. (1983b). Changes in plasma steroid hormone levels during gonadal maturation in female goldfishCarassius auratus. Bull. Jap. Soc. scient. Fish. 49: 1783–1789

    Google Scholar 

  • Kagawa, H., Young, G., Nagahama, Y. (1984). In vitro estradiol-17β and testosterone production by ovarian follicles of the goldfish,Carassius auratus. Gen. comp. Endocr. 54: 139–143

    Google Scholar 

  • Kobayashi, M., Aida, K., Hanyu, I. (1986). Annual changes in plasma levels of gonadotropin and steroid hormones in goldfish. Bull. Jap. Soc. scient. Fish. 52: 1153–1158

    Google Scholar 

  • Lam, T. J. (1983). Environmental influences on gonadal activity in fish. In: Hoar, W. S., Randall, D. J., Donaldson, E. M. (eds.) Fish physiology, Vol. IX B. Academic Press, New York, p. 65–116

    Google Scholar 

  • Lamba, V., Goswami, S. V., Sundararaj, B. I. (1983). Circannual and circadian variations in plasma levels of steroids (cortisol, estradiol-17β, estrone, and testosterone) correlated with the annual gonadal cycle in the catfish,Heteropneustes fossilis (Bloch). Gen. comp. Endocr. 50: 205–225

    Google Scholar 

  • Lambert, J. D. G., Bosman, G. I. C. G. M., Van den Hurk, R., Van Oordt, P. G. W. J. (1978). Annual cycle of plasma oestradiol-17β in the female troutSalmo gairdneri. Annls Biol. anim. Biochim. Biophys. 18: 923–927

    Google Scholar 

  • MacGregor, R., Dindo, J. J., Finucane J. H. (1981). Changes in serum androgens and estrogens during spawning in bluefish,Pomatomus saltator, and king mackerel,Scomberomorus cavalla. Can. J. Zool. 59: 1749–1754

    Google Scholar 

  • Matsuyama, M., Adachi, S., Nagahama, Y., Maruyama, K., Matsuura, S. (1990). Diurnal rhythm of serum steroid hormone levels in the Japanese whiting,Sillago japonica, a daily-spawning teleost. Fish Physiol. Biochem. 8: 329–338

    Google Scholar 

  • Matsuyama, M., Adachi, S., Nagahama, Y., Matsuura, S. (1988). Diurnal rhythm of oocyte development and plasma steroid hormone levels in the red sea bream,Pagrus major, during the spawning season. Aquaculture, Amsterdam 73: 357–372

    Google Scholar 

  • Nagahama, Y. (1987). Gonadotropin action on gametogenesis and steroidogenesis in teleost gonads. Zool. Sci. 4: 209–222

    Google Scholar 

  • Nagahama, Y., Adachi, S. (1985). Identification of maturation-inducing steroid in a teleost, the amago salmon (Oncorhynchus rhodurus). Devl Biol. 109: 428–435

    Google Scholar 

  • Nakai, Z. (1962). Studies of influences of environmental factors upon fertilization and development of the Japanese sardine eggs — with some reference to the number of their ova. Bull. Tokai reg. Fish. Res. Lab. 9: 109–150

    Google Scholar 

  • Nakai, Z., Usami, S. (1962). Seasonal fluctuation in the sexual maturity of the Japanese sardine. Bull. Tokai reg. Fish. Res. Lab. 9: 151–171 (in Japanese with English summary)

    Google Scholar 

  • Ouchi, K., Adachi, S., Nagahama, Y. (1988). Changes in plasma levels of steroid hormones during sexual maturation of female red seabreamPagrus major. Nippon Suisan Gakk. 54: 585–591 (in Japanese with English summary)

    Google Scholar 

  • Ouchi, K., Adachi, S., Nagahama, Y., Matsumoto, A. (1985). Ovarian maturity and plasma steroid hormone levels in the cultured and wild yellowtail (Seriola quinqueradiata) during spawning season. Bull. natn. Res. Inst. Aquaculture 7: 13–20 (in Japanese with English summary)

    Google Scholar 

  • Pankhurst, N. W. (1985). Final maturation and ovulation of oocytes of the goldeye,Hiodon alosoides (Rafinesque), in vitro. Can. J. Zool. 63: 1003–1009

    Google Scholar 

  • Pankhurst, N. W., Conroy, A. M. (1987). Seasonal changes in reproductive condition and plasma levels of sex steroids in the blue cod,Parapercis colias (Bloch and Schneider) (Mugiloididae). Fish Physiol. Biochem. 4: 15–26

    Google Scholar 

  • Pankhurst, N. W., Conroy, A. M. (1988). Endocrine changes during gonadal maturation and spawning in the orange roughy (Hoplostethus atlanticus Collett), a teleost from the midslope waters off New Zealand. Gen. comp. Endocr. 70: 262–273

    Google Scholar 

  • Pankhurst, N. W., Stacey, N. E., Van Der Kraak, G. (1986). Reproductive development and plasma levels of reproductive hormones of goldeye,Hiodon alosoides (Rafinesque), taken from the North Saskatchewan River during the open-water season. Can. J. Zool. 64: 2843–2849

    Google Scholar 

  • Rosenblum, P. M., Pudney, J., Callard, I. P. (1987). Gonadal morphology, enzyme histochemistry and plasma steroid levels during the annual reproductive cycle of male and female brown bullhead catfish,Ictalurus nebulosus Lesueur. J. Fish Biol. 31: 325–341

    Google Scholar 

  • Santos, A. J. G., Furukawa, K., Kobayashi, M., Bando, K., Aida, K., Hanyu, I. (1986). Plasma gonadotropin and steroid hormone profiles during ovulation in the carpCyprinus carpio. Bull. Jap. Soc. scient. Fish. 52: 1159–1166

    Google Scholar 

  • Scott, A. P., Bye, V. J., Baynes, S. M. (1980). Seasonal variations in sex steroids of female rainbow trout (Salmo gairdneri Richardson). J. Fish Biol. 17: 587–592

    Google Scholar 

  • Scott, A. P., Mackenzie, D. S., Stacey, N. E. (1984). Endocrine changes during natural spawning in the white sucker,Catostomus commersoni. II. Steroid hormones. Gen. comp. Endocr. 56: 349–359

    Google Scholar 

  • Scott, A. P., Sumpter, J. P. (1983). A comparison of the female reproductive cycles of autumn-spawning and winter-spawning strains of rainbow trout (Salmo gairdneri Richardson). Gen. comp. Endocr. 52: 79–85

    Google Scholar 

  • Scott, A. P., Sumpter, J. P., Hardiman, P. A. (1983). Hormone changes during ovulation in the rainbow trout (Salmo gairdneri Richardson). Gen. comp. Endocr. 49: 128–134

    Google Scholar 

  • Shimizu, A., Aida, K., Hanyu, I. (1985). Endocrine profiles during the short reproductive cycle of an autumn-spawning bitterling,Acheilognathus rhombea. Gen. comp. Endocr. 60: 361–371

    Google Scholar 

  • Stacey, N. E., Peter, R. E., Cook, A. F., Truscott, B., Walsh, J. M., Idler, D. R. (1983). Changes in plasma concentrations of gonadotropin, 17β-estradiol, testosterone, and 17α-hydroxy-20β-dihydroprogesterone during spontaneous and brain lesion induced ovulation in goldfish. Can. J. Zool. 61: 2646–2652

    Google Scholar 

  • Statistics and Informations Department, Ministry of Agriculture, Forestry and Fisheries (1990). Production of fisheries and water culture. In: The 63rd statistical yearbook of Ministry of Agriculture, Forestry and Fisheries, Japan, p. 262–263

    Google Scholar 

  • Trant, J. M., Thomas, P. (1988). Structure-activity relationships of steroids in inducing germinal vesicle breakdown of Atlantic croaker oocytes in vitro. Gen. comp. Endocr. 71: 307–317

    Google Scholar 

  • Trant, J. M., Thomas, P. (1989). Isolation of a novel maturation-inducing steroid produced in vitro by ovaries of Atlantic croaker. Gen. comp. Endocr. 75: 397–404

    Google Scholar 

  • Trant, J. M., Thomas, P., Shackleton, C. H. L. (1986). Identification of 17α,20β,21-trihydroxy-4-pregnen-3-one as the major ovarian steroid produced by the teleostMicropogonias undulatus during final oocyte maturation. Steroids 47: 89–99

    Google Scholar 

  • Truscott, B., Idler, D. R., So, Y. P., Walsh, J. M. (1986). Maturational steroids and gonadotropin in upstream migratory sockeye salmon. Gen. comp. Endocr. 62: 99–110

    Google Scholar 

  • Ueda, H., Hiroi, O., Hara, A., Yamauchi, K., Nagahama, Y. (1984). Changes in serum concentrations of steroid hormones, thyroxine, and vitellogenin during spawning migration of the chum salmon,Oncorhynchus keta. Gen. comp. Endocr. 53: 203–211

    Google Scholar 

  • Usami, S. (1964). Fecundity of the Japanese sardine,Sardinops melanosticta (Temminck & Schlegel) — I. Process of maturation and the number of ova determined on the basis of ovum diameter measurement of the large-sized females taken from the Japan Sea. Bull. Tokai reg. Fish. Res. Lab. 38: 1–30 (in Japanese with English summary)

    Google Scholar 

  • Usami, S. (1972). A note on sexual maturity of I-age sardine in the sea off Kanto District, Honshu, 1949 through 1951. Bull. Tokai reg. Fish. Res. Lab. 70: 25–36 (in Japanese with English summary)

    Google Scholar 

  • Van Ree, G. E., Lok, D., Bosman, G. (1977). In vitro induction of nuclear breakdown in oocytes of the zebrafishBrachydanio rerio (Ham. Buch.). Effects of the composition of the medium and of protein and steroid hormones. Proc. K. Ned. Akad. Wet. (Sect. C) 80: 353–371

    Google Scholar 

  • Whitehead, C., Bromage, N. R., Breton, B. (1983). Changes in serum levels of gonadotropin, oestradiol 17β and vitellogenin during the first and subsequent reproductive cycles of female rainbow trout. Aquaculture, Amsterdam 34: 317–326

    Google Scholar 

  • Wingfield, J. C., Grimm, A. S. (1977). Seasonal changes in plasma cortisol, testosterone and oestradiol-17β in the plaice,Pleuronectes platessa L. Gen. comp. Endocr. 31: 1–11

    Google Scholar 

  • Yamauchi, K., Kagawa, H., Ban, M., Kasahara, N., Nagahama, Y. (1984). Changes in plasma estradiol-17β and 17α,20β-dihy-droxy-4-pregnen-3-one levels during final oocyte maturation of the masu salmonOncorhynchus masou. Bull. Jap. Soc. scient. Fish. 50: 2137

    Google Scholar 

  • Young, G., Crim, L. W., Kagawa, H., Kambegawa, A., Nagahama, Y. (1983). Plasma 17α,20β-dihydroxy-4-pregnen-3-one levels during sexual maturation of amago salmon (Oncorhynchus rhodurus): correlation with plasma gonadotropin and in vitro production by ovarian follicles. Gen. comp. Endocr. 51: 96–105

    Google Scholar 

  • Young, G., Kagawa, H., Nagahama, Y. (1982). Secretion of aromatizableΔ 4 androgens by thecal layers during estradiol-17β production by ovarian follicles of amago salmon (Oncorhynchus rhodurus) in vitro. Biomed. Res. 3: 659–667

    Google Scholar 

  • Zhu, Y., Furukawa, K., Aida, K., Hanyu, I. (1989). Annual reproductive rhythm of the tobinumeri-dragonetRepromucennus beniteguri (Callionymidae) in Lake Hamana. Nippon Suisan Gakk. 55: 591–599

    Google Scholar 

  • Zohar, Y., Pagelson, G., Tosky, M. (1988). Daily changes in reproductive hormone levels in the female gilthead seabreamSparus aurata at the spawning period. In: Reproduction in fish — basic and applied aspects in endocrinology and genetics. Institut National de la Recherche Agronomique, Paris, p. 119–125

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Fish Propagation, Faculty of Bioresources, Mie University, 514, Kamihama, Tsu, Japan

    M. Matsuyama

  2. Laboratory of Reproductive Biology, National Institute for Basic Biology, 444, Okazaki, Japan

    S. Adachi & Y. Nagahama

  3. Department of Fisheries, Faculty of Agriculture, Kyushu University, Hakozaki, Higashi-ku, 812, Fukuoka, Japan

    C. Kitajima & S. Matsuura

Authors
  1. M. Matsuyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Adachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Y. Nagahama
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Kitajima
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Matsuura
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by M. Anraku, Tokyo

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matsuyama, M., Adachi, S., Nagahama, Y. et al. Annual reproductive cycle of the captive female Japanese sardineSardinops melanostictus: Relationship to ovarian development and serum levels of gonadal steroid hormones. Mar. Biol. 108, 21–29 (1991). https://doi.org/10.1007/BF01313467

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01313467

Keywords

Search

Navigation