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Correlation between the ovarian status and the androgen sensibility in the cultured Japanese eel, Anguilla japonica

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Abstract

Different responsive abilities of different types of eels (cultured, cultured feminized, and wild silver eels) during artificial maturation are recognized, and maturity status at the beginning of artificial maturation might be important. Maturity may represented by the distribution pattern of oocyte diameters. Androgens have been demonstrated to stimulate ovarian development in eels. To determine the initial status, operations were performed on eels to identify sex and to sample ovarian tissue. The recovered eels were then treated with 17α-methyltestosterone (17MT), and the responses of individual eels to 17MT were determined by the fold change in the mean oocyte diameter before and after treatment. Sampled ovarian tissues were fixed in Bouin’s solution, oocytes were isolated, and the diameter of isolated oocytes was measured. The ovarian status, determined by kernel density estimation (KDE), was presented by the probability density of measured oocyte diameters; compared with histograms, a description method, KDE, provided more subtle information on the investigated ovary. Our data indicated a correlation between the initial ovarian status (density pattern) and the consequence of treatment (change of ovary); we also argued the semelparity of the Japanese eel. Our results supported the hypothesis that the initial ovarian status is an important factor affecting artificial maturation and that androgens could ameliorate the initial status of the eel ovary.

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References

  • Arjona FJ, Vargas-Chacoff L, Martín Del Río MP, Flik G, Mancera JM, Klaren PHM (2011) Effects of cortisol and thyroid hormone on peripheral outer ring deiodination and osmoregulatory parameters in the Senegalese sole (Solea senegalensis). J Endocrinol 208:323–330

    CAS  PubMed  Google Scholar 

  • Hanel R, Stepputtis D, Bonhommeau S, Castonguay M, Schaber M, Wysujack K, Vobach M, Miller MJ (2014) Low larval abundance in the Sargasso Sea: new evidence about reduced recruitment of the Atlantic eels. Naturwissenschaften 101(12):1041–1054

    Article  CAS  Google Scholar 

  • Higuchi M, Mekuchi M, Hano T, Imaizumi H (2019) Trans-omics analyses revealed differences in hormonal and nutritional status between wild and cultured female Japanese eel (Anguilla japonica). PLoS One 14(5):e0209063. https://doi.org/10.1371/journal.pone.0209063

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang YS, Chen YM, Liao PC, Lee YH, Gwo JC, Chen MC, Chang CF (2012) Testosterone improves the transition of primary oocytes in artificial maturation eels (Anguilla japonica) by altering ovarian PTEN expression. Fish Physiol Biochem 38(3):777–787. https://doi.org/10.1007/s10695-011-9560-6

    Article  CAS  PubMed  Google Scholar 

  • Ijiri S, Kayaba T, Takeda N, Tachiki H, Adachi S, Yamauchi K (1998) Pretreatment reproductive stage and oocyte development induced by salmon pituitary homogenate in the Japanese eel Anguilla japonica. Fish Sci 64(4):531–537

    Article  CAS  Google Scholar 

  • Ijiri S, Tsukamoto K, Seinen Chow S, Kurogi H, Adachi S, Tanaka H (2011) Controlled reproduction in the Japanese eel (Anguilla japonica), past and present. Aquac Europe 36(2):13–17

    Google Scholar 

  • Kagawa H, Iinuma N, Tanaka H, Ohta H, Okuzawa K (1998) Effects of rearing period in seawater on induced maturation in female Japanese eel Anguilla japonica. Fish Sci 64(1):77–82

    Article  CAS  Google Scholar 

  • Kazeto Y, Ijiri S, Todo T, Adachi S, Yamauchi K (2000) Molecular cloning and characterization of Japanese eel ovarian P450c17 (CYP17) cDNA. Gen Comp Endocrinol 118:123–133

    Article  CAS  Google Scholar 

  • Kolli R, Cummings B, Glenn T, Bringolf R, Kenneke J (2017) Epigenetic mechanism mediating the regulation of the estrogen exposure biomarker vitellogenin in zebrafish. Gordon Research Conference on Cellular and Molecular Mechanisms of Toxicity, NH, Andover, August 13–18, 2017

  • Krzywinski M, Altman N (2013) Error bars. Nat Methods 10:921–922

    Article  CAS  Google Scholar 

  • Lai XJ, Li ZQ, Xie YJ, Chen SX, Wang YL (2018) Androstenedione and 17α-methyltestosterone induce early ovary development of Anguilla japonica. Theriogenology 120:16–24

    Article  CAS  Google Scholar 

  • Lee SC, Lou SW (2019) Androgenic modulation in the primary ovarian growth of the Japanese eel, Anguilla japonica. Zool Stud 58:2. https://doi.org/10.6620/ZS.2019.58-02

    Article  CAS  Google Scholar 

  • Lin HR, Zhang ML, Zhang SM, Van Der Kraak G, Peter RE (1991) Stimulation of pituitary gonadotropin and ovarian development by chronic administration of testosterone in female Japanese silver eel, Anguilla japonica. Aquaculture 96(1):87–95. https://doi.org/10.1016/0044-8486(91)90141-S

    Article  CAS  Google Scholar 

  • Lokman PM, Wylie MJ, Downes M, Di Biase A, Damsteegt EL (2015) Artificial induction of maturation in female silver eels, Anguilla australis: the benefits of androgen pre-treatment. Aquaculture 437:111–119

    Article  CAS  Google Scholar 

  • Misawa A, Kada S, Yoshida M (2014) Comparison of the mode of action of three anesthetic agents, 2-phenoxyethanol, MS-222, and eugenol on goldfish. Aquac Sci 62(4):425–432

    Google Scholar 

  • Monson C, Forsgren K, Goetz G, Harding L, Swanson P, Young G (2017) A teleost androgen promotes development of primary ovarian follicles in coho salmon and rapidly alters the ovarian transcriptome. Biol Reprod 97(5):731–745. https://doi.org/10.1093/biolre/iox124

    Article  PubMed  Google Scholar 

  • Mordenti O, Emmanuele P, Casalini A, Lokman PM, Zaccaroni A, Di Biase A, Parmeggiani A (2018) Effect of aromatable androgen (17-methyltestosterone) on induced maturation of silver European eels (Anguilla Anguilla): oocyte performance and synchronization. Aquac Res 49:442–448

    Article  CAS  Google Scholar 

  • Okamura A, Horie N, Mikawa N, Yamada Y, Tsukamoto K (2014) Recent advances in artificial production of glass eels for conservation of anguillid eel populations. Ecol Freshw Fish 23:95–110

    Article  Google Scholar 

  • Rattan S, Flaws JA (2019) The epigenetic impacts of endocrine disruptors on female reproduction across generations. Biol Reprod 101(3):635–644. https://doi.org/10.1093/biolre/ioz081

    Article  PubMed  Google Scholar 

  • Sudo R, Tosaka R, Ijiri S, Adachi S, Aoyama J, Tsukamoto K (2012) 11-ketotestosterone synchronously induces oocyte development and silvering-related changes in the Japanese eel, Anguilla japonica. Zool Sci 29(4):254–259

    Article  CAS  Google Scholar 

  • Tachiki H, Nakagawa T, Tamura K, Hirose K (1997) Effects of oral administration of estradiol-17 to young on gonadal sex and growth of Japanese eel Anguilla Japonica. Suisanzousyoku (水産増殖) 45(1):61–66 (in Japanese)

    CAS  Google Scholar 

  • Tanaka H, Kagawa H, Ohta H, Unuma T, Nomura K (2003) The first production of glass eel in captivity: fish reproductive physiology facilitates great progress in aquaculture. Fish Physiol Biochem 28:493–497

    Article  Google Scholar 

  • Tanaka S, Okamura A, Mikawa N, Yamada Y, Horie N, Utoh T, Zhang H, Oka HP, Tsukamoto K (2018) Development of oocytes in a post-spawning Japanese eel Anguilla japonica Temminck & Schlegel in captivity. bioRxiv. https://doi.org/10.1101/494435

  • Thorstad EB, Økland F, Westerberg H, Aarestrup K, Metcalfe JD (2013) Evaluation of surgical implantation of electronic tags in European eel and effects of different suture materials. Mar Freshw Res 64:324–331

    Article  CAS  Google Scholar 

  • Tsukamoto K, Chow S, Otake T, Kurogi H, Mochioka N, Miller MJ, Aoyama J, Kimura S, Watanabe S, Yoshinaga T, Shinoda A, Kuroki M, Oya M, Watanabe T, Hata K, Ijiri S, Kazeto Y, Nomura K, Tanaka H (2011) Oceanic spawning ecology of freshwater eels in the western North Pacific. Nature Communications 2(1):179. https://doi.org/10.1038/ncomms1174

  • Tzeng WN, Han YS, He JT (2002) The sex ratios and growth strategies of wild and captive Japanese eels Anguilla japonica. In: Small B, MacKinlay D (eds) Developments in understanding fish growth, symposium proceedings of international congress of the biology of fish, University of British Columbia. Vancouver B.C, Canada, pp 25–42

    Google Scholar 

  • Wang YS, Lou SW (2007) Influence of exogenous gonadotropin and sexual steroids on ovary development in Japanese eel, Anguilla japonica. J Fish Soc Taiwan 34:261–273. https://doi.org/10.29822/JFST.200709.0003

    Article  CAS  Google Scholar 

  • Walters KA, Middleton LJ, Joseph SR, Hazra R, Jimenez M, Simanainen U, Allan CM, Handelsman DJ (2012) Targeted loss of androgen receptor signaling in murine granulosa cells of preantral and antral follicles causes female subfertility. Biol Reprod 87(151):1–11

    Google Scholar 

  • Wand MP, Jones MC (1994) Kernel smoothing. Chapman & Hall/CRC monographs on statistics & applied probability (60). Boca Raton, FL, U.S.: Chapman & Hall

  • Zaroogian GE, Gutjahr-Gobell RE, Horowitz DB, Jayaraman S, Cantwell M, Chichester CO, Mills LJ (2012) Injectable, slow-release implantation method for exposing fish to chemicals over a period of weeks. N Am J Aquac 74(4):512–521

    Article  Google Scholar 

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Acknowledgments

We would like to thank Mr. Cheng Chang (Department of Life Science, NUK, Taiwan) for helping with the experimental manipulations, and Mr. YL Huang as well as Mr. YS Lei for their encouragement.

Funding

This study was partly funded by the Ministry of Science and Technology (MOST107-2321-B002-057), Taiwan.

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Authors and Affiliations

  1. Department of Life Science, National University of Kaohsiung, No.700, Kaohsiung University Road, Nan Tzu Dist, 811, Kaohsiung, Taiwan

    Yung-Sen Huang, Xuan-Hao Wu & Pei-Syuan Huang

  2. Freshwater Aquaculture Research Center, Fisheries Research Institute, C.O.A., No. 106, Haipu., 505., Changhua, Taiwan

    Guan-Ru Chen

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  1. Yung-Sen Huang
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  2. Xuan-Hao Wu
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  3. Pei-Syuan Huang
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  4. Guan-Ru Chen
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Correspondence to Yung-Sen Huang.

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Huang, YS., Wu, XH., Huang, PS. et al. Correlation between the ovarian status and the androgen sensibility in the cultured Japanese eel, Anguilla japonica. Fish Physiol Biochem 46, 1063–1074 (2020). https://doi.org/10.1007/s10695-020-00772-1

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