Diurnal Periodicity in Testicular Activity in the Japanese Flounder Paralichthys olivaceus

Michiya Matsuyama; Miki Yoneda; Hiroyuki Takeuchi; Hirohiko Kawaga; Masaaki Kashiwagi; Kazuo Tabata; Yoshitaka Nagahama; Shigeho Ijiri; Shinji Adachi; Kohei Yamauchi

doi:10.2331/fishsci.61.17

Diurnal Periodicity in Testicular Activity in the Japanese Flounder Paralichthys olivaceus

Michiya Matsuyama, Miki Yoneda, Hiroyuki Takeuchi, Hirohiko Kawaga, Masaaki Kashiwagi, Kazuo Tabata, Yoshitaka Nagahama, Shigeho Ijiri, Shinji Adachi, Kohei Yamauchi

Author information

Michiya Matsuyama
Faculty of Agriculture, Kyushu University
Miki Yoneda
Faculty of Bioresources, Mie University
Hiroyuki Takeuchi
Faculty of Bioresources, Mie University
Hirohiko Kawaga
National Research Institute of Aquaculture
Masaaki Kashiwagi
Faculty of Bioresources, Mie University
Kazuo Tabata
Hyogo Prefectural Fisheries Experimental Station
Yoshitaka Nagahama
National Institute for Basic Biology
Shigeho Ijiri
Faculty of Fisheries, Hokkaido University
Shinji Adachi
Faculty of Fisheries, Hokkaido University
Kohei Yamauchi
Faculty of Fisheries, Hokkaido University

Keywords: spermatogenesis, spermiation, steroid hormones, diuranal rhythm, Japanese flounder

JOURNAL FREE ACCESS

1995 Volume 61 Issue 1 Pages 17-23

DOI https://doi.org/10.2331/fishsci.61.17

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Published: 1995 Received: June 08, 1994 Available on J-STAGE: June 30, 2008 Accepted: - Advance online publication: - Revised: -
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Date of correction: June 30, 2008 Reason for correction: - Correction: CITATION Details: Wrong : 7 S. Adachi, S. Ijiri, K. Soyano, N. Takamaru, and K. Yamauchi: Proceedings of the Japan Society for Comparative Endocrinology, No. 6, p. 15 (1991).
1) Y. Nagahama: Gonadotropin action on gamategenesis and steroidogenesis in teleost gonads. Zool. Sci., 4, 209-222 (1987).
2) A. Fostier, F. Le Gac, and M. Loir: Steroids in male reproduction, in “Proc. IIIrd Int. Symp. Reprod. Physiol. Fish” (ed. by D. R. Idler,L. W. Crim, and J. M.Walsh), Memorial University of Newfoundland, St John's, 1987, pp. 239-245.
3) A. P. Scott and A. V. M. Canario: Status of oocyte maturationinducing steroids in teleosts, in “Proc. IIIrd Int. Symp. Reprod. Physiol. Fish” (ed. by D. R. Idler, L. W. Crim, and J. M. Walsh), Memorial University of Newfoundland, St John's, 1987, pp. 224-234.
4) T. Miura, K. Yamauchi, H. Takahashi, and Y. Nagahama: The role of hormones inthe acquisition of sperm motility in salmonid fish. J. expl Zool., 261, 359-363(1992).
5) R. Hirano and E. Yamamoto: Spawning rhythm and egg number at the individual female spawning experiment in the hirame flounder, Paralichthys olivaceus. Bull. Tottori. Pref. Fish. Exp. Stn., 33, 18-28 (1992) (in Japanese).
6) H. Kagawa, G. Young, S. Adachi, and Y. Nagahama: Estradiol-17β production inamago salmon (Oncorhynchus rhodurus) ovarian follicles: Role of the thecal and granulosa cells. Gen. Comp. Endocrinol., 47, 440-448 (1982).
7) G. Young, L. W. Crim, H. Kagawa, A. Kambegawa, and Y. Nagahama: 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. Endocrinol., 51, 96-105 (1983).
8) N. Sakai, H. Ueda, N. Suzuki, and Y. Nagahama: Steroid production by amago salmon testes at different development stages. Gen. Comp. Endocrinol., 75, 231-240 (1989).
9) T. Miura, K. Yamauchi, Y. Nagahama, and H. Takahashi: Induction of spermatogenesis in male Japanese eel, Anguilla japonica, by a single injection of human chorionic gonadotropin. Zool. Sci., 8, 63-73 (1991).
10) R. Billard, A. Fostier, C. Weil, and B. Breton: Endocrine control of spermatogenesis in teleost fish. Can. J. Fish. aquat Sci., 39, 65-79 (1982).
11) Y. Nagahama: The functional morphology of teleost gonads, in “Fish Physiology” (ed. by W. S. Hoar, D. J. Randall, and E. M. Donaldson), Vol. IXA, Academic Press, New York, 1983, pp. 223-276.
12) Y. Nagahama: Testis, in “Vertebrate Endocrinology: Application to Implications,” (ed. by P. K. T. Pang and M. P. Schreibman), Vol. 1, Academic Press, New York, 1986, pp. 399-437.
13) Y. Hiramoto and K. Kobayashi: Studies on the artificial reproduction of plaice, Paralichthys olivaceus (Temminck et Schlegel)-I. Spawning of the plaice cultured in an aquarium. The Aquiculture, 26, 152-158 (1979) (in Japanese).
14) T. P. Barry, A. J. G. Santos, K. Furukawa, K. Aida, and I. Hanyu: Steroid profiles during spawning in male common carp. Gen. Comp. Endocrinol., 80, 223-231 (1990).
15) H. Ueda, G. Young, L. W. Crim, A. Kambegawa, and Y. Nagahama: 17α, 20β-Dihydroxy-4-pregnen-3-one: plasma levels during sexualmaturation and in vitro production by the testes of amago salmon (Oncorhynchus rhodurus) and rainbow trout (Salmo gairdneri). Gen. Comp. Endocrinol., 51, 106-112 (1983).
16) H. Ueda, O. Hiroi, A. Hara, K. Yamauchi, and Y. Nagahama: Changes in serum concentrations of steroid hormones, thyroxine, and vitellogenin during spawning migration of the chum salmon, Oncorhynchus keta. Gen. Comp. Endocrinol., 53, 201-211 (1984).
17) H. M. Dye, J. P. Sumpter, U. H. M. Fagerland, and E. M. Donaldson: Changes in reproductive parameters during the spawning migration of pink salmon, Oncorhynchus gorbuscha (Walbaum). J. Fish Biol., 29, 167-176 (1986).
18) M. S. Fitzpatrick, G. Van Der Kraak, and C. B. Schreck: Profiles of plasma sex steroids and gonadotropin in coho salmon, Oncorhynchus kisutch, during final maturation. Gen. Comp. Endocrinol., 62, 437-451 (1986).
19) B. Truscott, D. R. Idler, Y. P. So, and J. M. Walsh: Maturational steroids and gonadotropin in upstream migratory sockeye salmon. Gen. Comp. Endocrinol., 62, 99-110 (1986).
20) A. P. Scott, D. S. Mackenzie, and N. E. Stacey: Endocrine changes during natural spawning in the white sucker, Catostomus commersoni II. Steroid hormones. Gen. Comp. Endocrinol., 56, 349-359 (1984).
21) M. Kobayashi, K. Aida, and I. Hanyu: Gonadotropin surge during spawning in male goldfish. Gen. Comp. Endocrinol., 62, 70-79 (1986).
22) N. W. Pankhurst, N. E. Stacey, and G. Van Der Kraak: 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 (1986).
23) N. W. Pankhurst and A. M. Conroy: Seasonal changes in re- productive condition and plasma levels of sex steroids in the blue cod, Parapercis colias (Bloch and Schneider) (Mugiloididae). Fish Physiol. Biochem., 4, 15-26 (1987).
24) K. Ouchi, S. Adachi, and Y. Nagahama: Changes in plasma levels of steroid hormones during sexual maturation of male red seabream Pagrus major. Nippon SuisanGakkaishi, 54, 593-597 (1988) (in Japanese).
25) M. Matsuyama, S. Adachi, Y. Nagahama, C. Kitajima, and S. Matsuura: Testicular development and serum levels of gonadal steroids during the annual reproductive cycle of captive Japanese sardine. Japan. J. Ichthyol, 37, 381-390 (1991).
26) M. Matsuyama, S. Adachi, Y. Nagahama, K. Maruyama, and S.Matsuura: Diurnal rhythm of serum steroid hormone levels in the Japanese whiting, Sillago japonica, a daily-spawning teleost. Fish Physiol. Biochem., 8, 329-338(1990).
27) K. Asahina, T. P. Barry, K. Aida, N. Fusetani, and I. Hanyu: Biosynthesis of 17α, 20α-dihydroxy-4-pregnen-3-one from 17a-hy-droxyprogesterone by spermatozoa of the common carp, Cyprinus carpio. J. expl Zool., 255, 244-249 (1990).
28) M. Kobayashi, K. Aida, and I. Hanyu: Effects of HCG on milt amount and plasma levels of steroid hormones in male goldfish. Nippon Suisan Gakkaishi, 52, 755 (1986).

Right : 1) Y. Nagahama: Gonadotropin action on gamategenesis and steroidogenesis in teleost gonads. Zool. Sci., 4, 209-222 (1987).
2) A. Fostier, F. Le Gac, and M. Loir: Steroids in male reproduction, in “Proc. IIIrd Int. Symp. Reprod. Physiol. Fish” (ed. by D. R. Idler,L. W. Crim, and J. M.Walsh), Memorial University of Newfoundland, St John's, 1987, pp. 239-245.
3) A. P. Scott and A. V. M. Canario: Status of oocyte maturationinducing steroids in teleosts, in “Proc. IIIrd Int. Symp. Reprod. Physiol. Fish” (ed. by D. R. Idler, L. W. Crim, and J. M. Walsh), Memorial University of Newfoundland, St John's, 1987, pp. 224-234.
4) T. Miura, K. Yamauchi, H. Takahashi, and Y. Nagahama: The role of hormones in the acquisition of sperm motility in salmonid fish. J. expl Zool., 261, 359-363(1992).
5) R. Hirano and E. Yamamoto: Spawning rhythm and egg number at the individual female spawning experiment in the hirame flounder, Paralichthys olivaceus. Bull. Tottori. Pref. Fish. Exp. Stn., 33, 18-28 (1992) (in Japanese).
6) H. Kagawa, G. Young, S. Adachi, and Y. Nagahama: Estradiol-17β production in amago salmon (Oncorhynchus rhodurus) ovarian follicles: Role of the thecal and granulosa cells. Gen. Comp. Endocrinol., 47, 440-448 (1982).
7) G. Young, L. W. Crim, H. Kagawa, A. Kambegawa, and Y. Nagahama: 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. Endocrinol., 51, 96-105 (1983).
8) N. Sakai, H. Ueda, N. Suzuki, and Y. Nagahama: Steroid production by amago salmon testes at different development stages. Gen. Comp. Endocrinol., 75, 231-240 (1989).
9) T. Miura, K. Yamauchi, Y. Nagahama, and H. Takahashi: Induction of spermatogenesis in male Japanese eel, Anguilla japonica, by a single injection of human chorionic gonadotropin. Zool. Sci., 8, 63-73 (1991).
10) R. Billard, A. Fostier, C. Weil, and B. Breton: Endocrine control of spermatogenesis in teleost fish. Can. J. Fish. aquat Sci., 39, 65-79 (1982).
11) Y. Nagahama: The functional morphology of teleost gonads, in “Fish Physiology” (ed. by W. S. Hoar, D. J. Randall, and E. M. Donaldson), Vol. IXA, Academic Press, New York, 1983, pp. 223-276.
12) Y. Nagahama: Testis, in “Vertebrate Endocrinology: Application to Implications,” (ed. by P. K. T. Pang and M. P. Schreibman), Vol. 1, Academic Press, New York, 1986, pp. 399-437.
13) Y. Hiramoto and K. Kobayashi: Studies on the artificial reproduction of plaice, Paralichthys olivaceus (Temminck et Schlegel)-I. Spawning of the plaice cultured in an aquarium. The Aquiculture, 26, 152-158 (1979) (in Japanese).
14) T. P. Barry, A. J. G. Santos, K. Furukawa, K. Aida, and I. Hanyu: Steroid profiles during spawning in male common carp. Gen. Comp. Endocrinol., 80, 223-231 (1990).
15) H. Ueda, G. Young, L. W. Crim, A. Kambegawa, and Y. Nagahama: 17α, 20β-Dihydroxy-4-pregnen-3-one: plasma levels during sexualmaturation and in vitro production by the testes of amago salmon (Oncorhynchus rhodurus) and rainbow trout (Salmo gairdneri). Gen. Comp. Endocrinol., 51, 106-112 (1983).
16) H. Ueda, O. Hiroi, A. Hara, K. Yamauchi, and Y. Nagahama: Changes in serum concentrations of steroid hormones, thyroxine, and vitellogenin during spawning migration of the chum salmon, Oncorhynchus keta. Gen. Comp. Endocrinol., 53, 201-211 (1984).
17) H. M. Dye, J. P. Sumpter, U. H. M. Fagerland, and E. M. Donaldson: Changes in reproductive parameters during the spawning migration of pink salmon, Oncorhynchus gorbuscha (Walbaum). J. Fish Biol., 29, 167-176 (1986).
18) M. S. Fitzpatrick, G. Van Der Kraak, and C. B. Schreck: Profiles of plasma sex steroids and gonadotropin in coho salmon, Oncorhynchus kisutch, during final maturation. Gen. Comp. Endocrinol., 62, 437-451 (1986).
19) B. Truscott, D. R. Idler, Y. P. So, and J. M. Walsh: Maturational steroids and gonadotropin in upstream migratory sockeye salmon. Gen. Comp. Endocrinol., 62, 99-110 (1986).
20) A. P. Scott, D. S. Mackenzie, and N. E. Stacey: Endocrine changes during natural spawning in the white sucker, Catostomus commersoni II. Steroid hormones. Gen. Comp. Endocrinol., 56, 349-359 (1984).
21) M. Kobayashi, K. Aida, and I. Hanyu: Gonadotropin surge during spawning in male goldfish. Gen. Comp. Endocrinol., 62, 70-79 (1986).
22) N. W. Pankhurst, N. E. Stacey, and G. Van Der Kraak: 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 (1986).
23) N. W. Pankhurst and A. M. Conroy: 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 (1987).
24) K. Ouchi, S. Adachi, and Y. Nagahama: Changes in plasma levels of steroid hormones during sexual maturation of male red seabream Pagrus major. Nippon Suisan Gakkaishi, 54, 593-597 (1988) (in Japanese).
25) M. Matsuyama, S. Adachi, Y. Nagahama, C. Kitajima, and S. Matsuura: Testicular development and serum levels of gonadal steroids during the annual reproductive cycle of captive Japanese sardine. Japan. J. Ichthyol, 37, 381-390 (1991).
26) M. Matsuyama, S. Adachi, Y. Nagahama, K. Maruyama, and S.Matsuura: Diurnal rhythm of serum steroid hormone levels in the Japanese whiting, Sillago japonica, a daily-spawning teleost. Fish Physiol. Biochem., 8, 329-338(1990).
27) K. Asahina, T. P. Barry, K. Aida, N. Fusetani, and I. Hanyu: Biosynthesis of 17α, 20α-dihydroxy-4-pregnen-3-one from 17α-hy-droxyprogesterone by spermatozoa of the common carp, Cyprinus carpio. J. expl Zool., 255, 244-249 (1990).
28) M. Kobayashi, K. Aida, and I. Hanyu: Effects of HCG on milt amount and plasma levels of steroid hormones in male goldfish. Nippon Suisan Gakkaishi, 52, 755 (1986).

Date of correction: June 30, 2008 Reason for correction: - Correction: PDF FILE Details: -

Abstract

Testicular activity, as represented by the amount of each type of testicular germ cell in the seminal lobules, and the serum levels of three major male teleost steroids-testosterone (T), 11-ketotestosterone (11-KT), and 17α, 20β-dihydroxy-4-pregnen-3-one (17α, 20β-DP) -were investigated during the daily spawning cycle of the male Japanese flounder Paralichthys olivaceus.
B-type spermatogonia and spermatocytes increased in number from the lowest level at 22:00 (186 cells/lobule), and peaked at 10:00 (292 cells/lobule). The number of spermatozoa increased from 14:00 (370cells/lobule) and peaked at 22:00 (782 cells/lobule). In contrast, spermatid numbers decreased from 14:00 (579 cells/lobule) and showed the lowest level at 22:00 (348 cells/lobule). These results indicate that spermatogenesis (spermatogonial proliferation, the formation of spermatocytes and spermatids) occurs between 22:00 and 10:00, and spermiation (release of spermatozoa into the lobular lumen from the cysts) occurs between 14:00 and 22:00. Thus, spermatogenesis and spermiation occur on a daily basis in the male Japanese flounder. Serum T and 11-KT levels showed no significant fluctuation throughout the day. Serum 17α, 20β-DP was maintained at a low or undetectable level throughout the experimental period, but showed a surge (110 pg/m/) at 22:00. This short-lived 17α, 20β-DP surge corresponded to the peak of spermiation. This study demonstrates, therefore, the existence of a diurnal periodicity in (1) spermatogenesis and spermiation, and (2) 17α, 20β-DP production.

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