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Suppression of male reproductive activity by estradiol in goldfish: appearance of infertile males that perform active spawning behavior

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Abstract

Estrogenic endocrine-disrupting chemicals are an increasing social concern, as they can reduce the reproductive activity of wildlife. The present study aimed to clarify the long-term effects of estradiol-17β (E2) on male reproductive activity in goldfish. Sexually mature male goldfish were implanted with a silicone capsule containing E2, and kept for 14 weeks or 15 weeks. The reproductive activity of these fish was individually traced. The percentage of fish with tubercles on opercula and pectoral fins and expressible milt started to decrease at 5 weeks after capsule implantation and remained at low levels. Inhibition of spawning activity by E2 occurred later than inhibition of the development of tubercles and milt production. Thirty percent of E2-treated fish showed no spawning at 15 weeks, whereas 70% of fish showed active spawning. The relationship between milt production and spawning activity revealed that some E2-treated fish performed active spawning behavior with no expressible milt because of the time lag of suppression between milt production and spawning activity. Therefore, environmental estrogen does not simply cause non-spawning males, but can also cause behaviorally active infertile males, which leads to failure of egg fertilization, resulting in a substantial decrease in population size in wild fish.

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References

  • Allen Y, Scott AP, Matthiessen P, Haworth S, Thain JE, Feist S (1999) Survey of estrogenic activity in United Kingdom estuarine and coastal waters and its effects on gonadal development of the flounder Platichthys flesus. Environ Toxicol Chem 18:1791–1800

    Article  CAS  Google Scholar 

  • Bayley M, Nielsen JR, Baatrup E (1999) Guppy sexual behavior as an effect biomarker of estrogen mimics. Ecotoxicol Environ Safety 43:68–73

    Article  CAS  Google Scholar 

  • Bhandari RK, Deem SL, Holliday DK, Jandegian CM, Kassortis CD, Nagel SC, Tillitt DE, vom Saal FS, Rosenfeld CS (2015) Effects of the environmental estrogenic contaminants bisphenol A and 17μ-ethinyl estradiol on sexual development and adult behaviors in aquatic wildlife species. Gen Comp Endocrinol 214:195–219

    Article  CAS  Google Scholar 

  • Billard R, Breton B, Richard M (1981) On the inhibitory effect of some steroids on spermatogenesis in adult rainbow trout (Salmo gairdneri). Can J Zool 59:1479–1487

    Article  CAS  Google Scholar 

  • Bjerselius R, Lundstedt-Enkel K, Olsen H, Mayer I, Dimberg K (2001) Male goldfish reproductive behavior and physiology are severely affected by exogenous exposure to 17μ-estradiol. Aquat Toxicol 53:139–152

    Article  CAS  Google Scholar 

  • Colborn T, Dumanoski D, Myers JP (1996) Our stolen future. Penguin Books USA Inc, New York

    Google Scholar 

  • Fang TY, Praveena SM, Aris AZ, Ismail SNS, Rasdi I (2019) Quantification of selected steroid hormones (17μ-estradiol and 17μ-ethynylestradiol) in wastewater treatment plants in Klang Valley (Malaysia). Chemosphere 215:153–162

    Article  Google Scholar 

  • Gong J, Ran Y, Zhang D, Chen D, Li H, Huang Y (2019) Vertical profiles and distributions of aqueous endocrine-disrupting chemicals in different matrices from the pearl river delta and the influence of environmental factors. Environ Pollution 246:328–335

    Article  CAS  Google Scholar 

  • Hashimoto S, Bessho H, Hara A, Nakamura M, Iguchi T, Fujita K (2000) Elevated serum vitellogenin levels and gonadal abnormalities in wild male flounder (Pleuronectes yokohamae) from Tokyo Bay, Japan. Mar Environ Res 49:37–53

    Article  CAS  Google Scholar 

  • Howell WM, Black DA, Bortone SA (1980) Abnormal expression of secondary sex characters in a population of mosquitofish, Gambusia affinis holbrooki: evidence for environmentally-induced masculinization. Copeia 1980:676–681

    Article  Google Scholar 

  • Iwata E, Nagai Y, Hyoudou M, Sasaki H (2008) Social environment and sex differentiation in false clown anemonefish, Amphiprion ocellaris. Zool Sci 25:123–128

    Article  Google Scholar 

  • Iwata E, Suzuki N, Ohno S (2019) Influence of social stability on the sex determination process in false clown anemonefish (Amphiprion ocellaris). Marine Freshwater Behav Physiol 52:107–119

    Article  CAS  Google Scholar 

  • Jobling S, Nolan M, Tyler CR, Brighty G, Sumpter JP (1998) Widespread sexual disruption in wild fish. Environ Sci Technol 22:2498–2506

    Article  Google Scholar 

  • Kawaguchi Y, Nagaoka A, Kitami A, Mitsuhashi T, Hayakawa Y, Kobayashi M (2014) Gender-typical olfactory regulation of sexual behavior in goldfish. Front Neurosci. https://doi.org/10.3389/fnins.2014.0091

    Article  PubMed  PubMed Central  Google Scholar 

  • Kime DE (1998) Endocrine disruption in fish. Kluwer Academic Publishers, Boston

    Book  Google Scholar 

  • Kobayashi M, 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

    Article  CAS  Google Scholar 

  • Kobayashi M, Aida K, Hanyu I (1986a) Gonadotropin surge during spawning in male goldfish. Gen Comp Endocrinol 62:70–79

    Article  CAS  Google Scholar 

  • Kobayashi M, Aida K, Hanyu Y (1986b) Annual changes in plasma levels of gonadotropin and steroid hormones in goldfish. Nippon Suisan Gakkaishi 52:1153–1158

    Article  CAS  Google Scholar 

  • Kobayashi M, Aida K, 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

    Article  CAS  Google Scholar 

  • Kobayashi M, Aida K, Hanyu Y (1988) Hormone changes during ovulatory cycle in goldfish. Gen Comp Endocrinol 69:301–307

    Article  CAS  Google Scholar 

  • Kobayashi M, Aida K, Hanyu Y (1989) Induction of gonadotropin surge by steroid hormone implantation in ovariectomized and sexually regressed female goldfish. Gen Comp Endocrinol 73:469–476

    Article  CAS  Google Scholar 

  • Martinovic D, Hogarth WT, Jones RE, Sorensen PW (2007) Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows. Environ Toxicol Chem 26:271–278

    Article  CAS  Google Scholar 

  • Miura T, Miura C, Ohta T, Nader MR, Todo T, Yamauchi K (1999) Estradiol-17α stimulates the renewal of spermatogonial stem cells in males. Biochem Biophys Res Commun 264:230–234

    Article  CAS  Google Scholar 

  • Munakata A, Kobayashi M (2010) Endocrine control of sexual behavior in teleost fish. Gen Comp Endocrinol 165:456–468

    Article  CAS  Google Scholar 

  • Oshima Y, Kang IJ, Kobayashi M, Nakayama K, Imada N, Honjo T (2003) Suppression of sexual behavior in male Japanese medaka (Oryzias latipes) exposed to 17β-estradiol. Chemosphere 50:429–436

    Article  Google Scholar 

  • Paraso MGV, Morales JKC, Clavecillas AA, Lola MSEG (2017) Estrogenic effects in feral male common carp (Cyprinus carpio) from Laguna de Bay, Philippines. Bull Environ Contam Toxicol 98:638–642

    Article  CAS  Google Scholar 

  • Pena-Guzman C, Ulloa-Sanchez S, Mora K, Helena-Bustos R, Lopez-Barrera E, Alvarez J, Rodriguez-Pinzon M (2019) Emerging pollutants in the urban water cycle in Latin America: a review of the current literature. J Environ Manage 237:408–423

    Article  CAS  Google Scholar 

  • Saaristo M, Johnstone CP, Xu K, Allinson M, Wong BBM (2019) The endocrine disruptor, 17α -ethinyl estradiol, alters male mate choice in a freshwater fish. Aquat Toxicol 208:118–125

    Article  CAS  Google Scholar 

  • Saoshiro S, Kawaguchi Y, Hayakawa Y, Kobayashi M (2013) Sexual bipotentiality of behavior in male and female goldfish. Gen Comp Endocrinol 181:265–270

    Article  CAS  Google Scholar 

  • Schoenfuss H, Levitt JT, Van Der Kraak G, Sorensen PW (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

    Article  CAS  Google Scholar 

  • Schuster AC, Rodrigues GZP, Zwetsch BG, Garcia ALH, Gehlen G (2019) 17β-ethinyl estradiol induces behavioral and reproductive damages in zebrafish (Danio rerio). Ecotoxicol Environ Contam 14:59–64

    Google Scholar 

  • Shinohara Y, Kobayashi M (2020) Sexual bipotentiality of the olfactory pathway for sexual behavior in goldfish. Fish Sci 86:819–827

    Article  CAS  Google Scholar 

  • Stacey N, Kobayashi M (1996) Androgen induction of male sexual behaviors in female goldfish. Horm Behav 30:434–445

    Article  CAS  Google Scholar 

  • Trudeau VL, Peter RE, Sloley BD (1991) Testosterone and estradiol potentiate the serum gonadotropin response to gonadotropin-releasing hormone in goldfish. Biol Reprod 44:951–960

    Article  CAS  Google Scholar 

  • Trudeau VL, Wade MG, Van Der Kraak G, Peter RE (1993) Effects of 17β-estradiol on pituitary and testicular function in male goldfish. Can J Zool 71:1131–1136

    Article  CAS  Google Scholar 

  • Vajda AM, Norris DO (2011) Endocrine-active chemicals (EACs) in fish. In: Norris DO, Lopez KH (eds) Hormones and reproduction of vertebrates, vol 1. Fishes. Academic Press, London, pp 245–264

    Google Scholar 

  • Van Aerle R, Nolan M, Jobling S, Christiansen LB, Sumpter JP (2001) Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ Toxicol Chem 20:2841–2847

    Article  Google Scholar 

  • Weber AA, Moreira DP, Melo RMC, Ribeiro YM, Bazzoli N, Rizzo E (2019) Environmental exposure to oestrogenic endocrine disruptors mixtures reflecting on gonadal sex steroids and gametogenesis of the neotropical fish Astynax rivularis. Gen Comp Endocrinol 279:99–108

    Article  CAS  Google Scholar 

  • Xu EG, Chan SN, Choi KW, Lee JHW, Leung KMY (2018) Tracking major endocrine disruptors in coastal waters using an integrating approach coupling field-based study and hydrodynamic modeling. Environ Pollution 233:387–394

    Article  CAS  Google Scholar 

  • Zheng S, Mo J, Wang Y, Ni C, Li X, Zhu Q, Ge RS (2019) Endocrine disruptors of inhibiting testicular 3μ-hydroxysteroid dehydrogenase. Chemico-Biol Interact 303:90–97

    Article  Google Scholar 

Download references

Acknowledgements

We thank Professor Hirohiko Kagawa of Miyazaki University and Dr. Masaru Nakamura of Okinawa Churashima Research Center for their critical comments on the histology of the testes of goldfish. We thank Professor Ryosuke Fujinuma of International Christian University for his critical reading of the manuscript.

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Correspondence to Makito Kobayashi.

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Kobayashi, M., Kijima, M., Matsuzuka, Y. et al. Suppression of male reproductive activity by estradiol in goldfish: appearance of infertile males that perform active spawning behavior. Fish Sci 87, 93–104 (2021). https://doi.org/10.1007/s12562-020-01487-1

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