Skip to main content

Comparative responses in rare minnow exposed to 17β-estradiol during different life stages

Abstract

Present in the excrement of humans and animals, 17β-estradiol (E2) has been detected in the aquatic environment in a range from several nanograms to several hundred nanograms per liter. In this study, the sensitivities of rare minnows during different life stages to E2 at environmentally relevant (5, 25, and 100 ng l−1) and high (1000 ng l−1) concentrations were compared using vitellogenin (VTG) and gonad development as biomarkers under semistatic conditions. After 21 days of exposure, VTG concentrations in whole-body homogenates were analyzed; the results indicated that the lowest observed effective concentration for VTG induction was 25 ng l−1 E2 in the adult stage, but 100 ng l−1 E2 in the larval and juvenile stages. After exposure in the early life stage, the larval and juvenile fish were transferred to clean water until gonad maturation. No significant difference in VTG induction was found between the exposure and control groups in the adults. However, a markedly increased proportion of females and appearance of hermaphrodism were observed in the juvenile-stage group exposed to 25 ng l−1 E2. These results showed that VTG induction in the adult stage is more sensitive than in larval and juvenile stages following exposure to E2. The juvenile stage may be the critical period of gonad development. Sex ratio could be a sensitive biomarker indicating exposure to xenoestrogens in early-life-stage subchronic exposure tests. The results of this study provide useful information for selecting sensitive biomarkers properly in aquatic toxicology testing.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

dph:

Days post hatch

LOEC:

Lowest observed effect concentration

E1 :

Estrone

VTG:

Vitellogenin

E2 :

17β-Estradiol

WBH:

Whole-body homogenates

EDCs:

Endocrine disrupter chemicals

ELISA:

Enzyme-linked immunosorbent assay

References

  • Aguayo S, Munoz MJ, de la Torre A et al (2004) Identification of organic compounds and ecotoxicological assessment of sewage treatment plants (STP) effluents. Sci Total Environ 328:69–81. doi:10.1016/j.scitotenv.2004.02.013

    Article  PubMed  CAS  Google Scholar 

  • Andersen L, Petersen GI, Gessbo Å et al (2001) Zebrafish (Danio rerio) and roach (Rutilus rutilus)—two species suitable for evaluating effects of endocrine disrupting chemicals? Aquat Ecosyst Health Manage 4:275–282. doi:10.1080/146349801753509177

    Article  CAS  Google Scholar 

  • Andersen LA, Holbech H, Gessbo Å et al (2003) Effects of exposure to 17α-ethynylestradiol during early development on sexual differentiation and induction of vitellogenin in zebrafish (Danio rerio). Comp Biochem Physiol C 134:365–374

    Article  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 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  PubMed  CAS  Google Scholar 

  • Brion F, Tyler CR, Palazzi X et al (2004) Impacts of 17β-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult-life stages in Zebrafish (Danio rerio). Aquat Toxicol 68:193–217. doi:10.1016/j.aquatox.2004.01.022

    Article  PubMed  CAS  Google Scholar 

  • Carballo M, Aguayo S, de la Torre A et al (2005) Plasma vitellogenin levels and gonadal morphology of wild carp (Cyprinus carpio L.) in a receiving rivers downstream of sewage treatment plants. Sci Total Environ 341:71–79. doi:10.1016/j.scitotenv.2004.08.021

    Article  PubMed  CAS  Google Scholar 

  • Colborn T, Dumanoski D, Myers JP (1996) Our stolen future. Dutton, New York

    Google Scholar 

  • Desbrow C, Routledge EJ, Brighty GC et al (1998) Identification of estrogenic chemicals in STW effluent. I: chemical fractionation and in vitro biological screening. Environ Sci Technol 32:1549–1558. doi:10.1021/es9707973

    Article  CAS  Google Scholar 

  • Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364. doi:10.1016/S0044-8486(02)00057-1

    Article  CAS  Google Scholar 

  • Dizer H, Fischer B, Sepulveda I et al (2002) Estrogenic effect of leachates and soil extracts from lysimeters spiked with sewage sludge and reference endocrine disrupters. Environ Toxicol 17:105–112. doi:10.1002/tox.10038

    Article  PubMed  CAS  Google Scholar 

  • Folmar LC, Hemmer MJ, Denslow ND et al (2002) A comparison of the estrogenic potencies of estradiol, ethynylestradiol, diethylstilbestrol, nonylphenol and methoxychlor in vivo and in vitro. Aquat Toxicol 60:101–110. doi:10.1016/S0166-445X(01)00276-4

    Article  PubMed  CAS  Google Scholar 

  • Folmar LC, Hemmer M, Hemmer R et al (2000) Comparative estrogenicity of estradiol, ethynyl estradiol and diethylstilbestrol in an in vivo, male sheepshead minnow (Cyprinodon variegatus), vitellogenin bioassay. Aquat Toxicol 49:77–88. doi:10.1016/S0166-445X(99)00076-4

    Article  PubMed  CAS  Google Scholar 

  • Hsiao CD, Tsai HJ (2003) Transgenic zebrafish with fluorescent germ cell: a useful tool to visualize germ cell proliferation and juvenile hermaphroditism in vivo. Dev Biol 262:313–323. doi:10.1016/S0012-1606(03)00402-0

    Article  PubMed  CAS  Google Scholar 

  • Jin SW, Xu Y, Hui Y et al (2005) Quantitative determination of 8 kinds of estrogenic compound in wastewater. China Water Wastewater 21:94–97

    CAS  Google Scholar 

  • Jobling S, Tyler CR (2006) Introduction: the ecological relevance of chemically induced endocrine disruption in wildlife. Environ Health Perspect 114(S1):7–8. doi:10.1289/ehp.8050

    Article  PubMed  Google Scholar 

  • Johnson AC, Aerni HR, Gerritsen A et al (2005) Comparing steroid estrogen, and nonylphenol content across a range of European sewage plants with different treatment and management practices. Water Res 39:47–58. doi:10.1016/j.watres.2004.07.025

    Article  PubMed  CAS  Google Scholar 

  • Kavlock RJ, Daston GP, de Rosa C et al (1996) Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop. Environ Health Perspect 104:715–740. doi:10.2307/3432708

    Article  PubMed  Google Scholar 

  • Koger CS, Teh SJ, Hinton DE (2000) Determining the sensitive developmental stages of intersex induction in medaka (Oryzias latipes) exposed to 17-beta-estradiol or testosterone. Mar Environ Res 50:201–206. doi:10.1016/S0141-1136(00)00068-4

    Article  PubMed  CAS  Google Scholar 

  • Komen J, Lambert JGD, Richter CJJ et al (1995) Endocrine control of sex differentiation in XX female, and in XY and XX male common carp (Cyprinus carpio L.). Proceedings of the fifth international symposium on the reproductive physiology of fish. Fish Symposium 95, Austin, TX, USA, p 383

  • Länge R, Hutchinson TH, Croudace CP et al (2001) Effects of the synthetic estrogen 17-alpha-ethinylestradiol on the life-cycle of the Fathead Minnow (Pimephales promelas). Environ Toxicol Chem 20:1216–1227. doi :10.1897/1551-5028(2001)020<1216:EOTSEE>2.0.CO;2

    Article  PubMed  Google Scholar 

  • Legler J, Broekhof JLM, Brouwer A et al (2000) A novel in vivo bioassay for (xeno-) estrogens using transgenic zebrafish. Environ Sci Technol 34:4439–4444. doi:10.1021/es0000605

    Article  CAS  Google Scholar 

  • Liao T, Jin SW, Yang FX et al (2006) An enzyme-linked immunosorbent assay for rare minnow (Gobiocypris rarus) vitellogenin and comparison of vitellogenin responses in rare minnow and zebrafish (Danio rerio). Sci Total Environ 364:284–294. doi:10.1016/j.scitotenv.2006.02.028

    Article  CAS  Google Scholar 

  • Lu L, Shen YW (2002) Acute toxicity of phenol, alkylbenzene, nitrobenzene and water sample to sword fish (Xiphorus helleri) and rare minnow (Gobiocypris rarus). Res Environ Sci 15:57–59

    Google Scholar 

  • Nath P, Sahu R, Kabita SK et al (2007) Vitellogenesis with special emphasis on Indian fishes. Fish Physiol Biochem 33:359–366. doi:10.1007/s10695-007-9167-0

    Article  CAS  Google Scholar 

  • Panter GH, Thompson RS, Sumpter JP (1998) Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural oestrogens, oestradiol and oestrone. Aquat Toxicol 42:243–253. doi:10.1016/S0166-445X(98)00038-1

    Article  CAS  Google Scholar 

  • Piferrer F (2001) Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197:229–281. doi:10.1016/S0044-8486(01)00589-0

    Article  CAS  Google Scholar 

  • Re MR, Fu TY (1983) Description of a new genus and species of Danioninae from China. Acta Zootaxonomica Sin 8:434–437

    Google Scholar 

  • Rodgers-Gray TP, Jobling S, Kelly C et al (2001) Exposure of juvenile roach (Rutilus rutilus) to treated sewage effluent induces dose-dependent and persistent disruption in gonadal duct development. Environ Sci Technol 35:462–470. doi:10.1021/es001225c

    Article  PubMed  CAS  Google Scholar 

  • Routledge EJ, Sheahan D, Desbrow C et al (1998) Identification of estrogenic chemicals in STW effluent. 2. In vivo responses in trout and roach. Environ Sci Technol 32:1559–1565. doi:10.1021/es970796a

    Article  CAS  Google Scholar 

  • Segner H, Caroll K, Fenske M et al (2003) Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicol Environ Saf 54:302–314. doi:10.1016/S0147-6513(02)00039-8

    Article  PubMed  CAS  Google Scholar 

  • Servos MR, Bennie DT, Burnison BK et al (2005) Distribution of estrogens, 17β-estradiol and estrone, in Canadian municipal wastewater treatment plants. Sci Total Environ 336:155–170. doi:10.1016/j.scitotenv.2004.05.025

    Article  PubMed  CAS  Google Scholar 

  • Shore LS, Gurevitz M, Shemesh M (1993) Estrogen as an environmental pollutant. Bull Environ Contam Toxicol 51:361–366. doi:10.1007/BF00201753

    Article  PubMed  CAS  Google Scholar 

  • Snyder SA, Keith TL, Verbrugge DA et al (1999) Analytical methods for detection of selected estrogenic compounds in aqueous mixtures. Environ Sci Technol 33:2814–2820. doi:10.1021/es981294f

    Article  CAS  Google Scholar 

  • Soto AM, Sonnenschein C, Chung KL et al (1995) The E-screen assay as a tool to identify estrogens: an update on estrogenic environment pollutants. Environ Health Perspect 103(S7):113–122. doi:10.2307/3432519

    Article  PubMed  CAS  Google Scholar 

  • Sumpter JP, Jobling S (1995) Vitellogenin as a biomarker for oestrogenic contamination of the aquatic environment. Environ Health Perspect 103:173–178. doi:10.2307/3432529

    Article  PubMed  CAS  Google Scholar 

  • Thorpe KL, Hetheridge MJ, Hutchinson TH et al (2001) Assessing the biological potency of binary mixtures of environmental estrogens using vitellogenin induction in juvenile rainbow trout (Oncorhynchus mykiss). Environ Sci Toxicol 35:2476–2481

    CAS  Google Scholar 

  • Tyler CR, van Aerle R, Hutchinson TH et al (1999) An in vivo testing system for endocrine disruptors in fish early life stages using induction of vitellogenin. Environ Toxicol Chem 18:337–347. doi :10.1897/1551-5028(1999)018<0337:AIVTSF>2.3.CO;2

    Article  CAS  Google Scholar 

  • Ünal G, Türkoğlu V, Oğuz AR et al (2007) Gonadal histology and some biochemical characteristics of Chalcalburnus tarichi (Pallas, 1811) having abnormal gonads. Fish Physiol Biochem 33:153–165. doi:10.1007/s10695-006-9126-1

    Article  CAS  Google Scholar 

  • U.S. Environmental Protection Agency Strategic plan for the Office of Research and Development. EPA/600/R3-91-063; 1996. Washington, DC, USA

  • U.S. Environmental Protection Agency a Short-Term Test Method for Assessing the Reproductive toxicity of Endocrine-Disrupting Chemicals Using the Fathead Minnow (Pimephales promelas). EPA/600/R-01/067; 2002. Washington, DC, USA

  • Van den Belt K, Berckmans P, Vangenechten C et al (2004) Comparative study on the in vitro/in vivo estrogenic potencies of 17β-estradiol, estrone, 17α-ethynylestradiol and nonylphenol. Aquat Toxicol 66:183–195. doi:10.1016/j.aquatox.2003.09.004

    Article  PubMed  CAS  Google Scholar 

  • Wang JW (1999) Spawning performance and development of oocytes in Gobiocypris rarus. Acta Hydrobiologica Sin 23:161–166

    CAS  Google Scholar 

  • Yamamoto T (1975) Medaka (Killifish): biology and strains. Keigaku Pub. Co., Tokyo

    Google Scholar 

  • Zha JM, Wang ZJ, Wang N et al (2007) Histological alternation and vitellogenin induction in adult rare minnow (Gobiocypris rarus) after exposure to ethynylestradiol and nonylphenol. Chemosphere 66:488–495. doi:10.1016/j.chemosphere.2006.05.071

    Article  PubMed  CAS  Google Scholar 

  • Zha JM, Sun LW, Zhou YQ et al (2008) Assessment of 17α-ethinylestradiol effects and underlying mechanisms in a continuous, multigeneration exposure of the Chinese rare minnow (Gobiocypris rarus). Toxicol Appl Pharmacol 226:298–308. doi:10.1016/j.taap. 2007.10.006

    Article  PubMed  CAS  Google Scholar 

  • Zhong XP, Xu Y, Liang Y et al (2004) Vitellogenin in rare minnow (Gobiocypris rarus): identification and induction by waterborne diethylstilbestrol. Comp Biochem Physiol C 137:291–298

    Google Scholar 

  • Zhou QF, Jiang GB, Liu JY (2002) Effects of sublethal levels of tributyltin chloride in a new toxicity test organism: the chinese rare minnow (Gobiocypris rarus). Arch Environ Contam Toxicol 42:332–337. doi:10.1007/s00244-001-0014-5

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors express sincere thanks for the financial support from Hi-Tech Research and Development Program of China (2006AA06Z424) and National Basic Research Program of China (2003CB415005) for this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Y. Xu.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Liao, T., Guo, Q.L., Jin, S.W. et al. Comparative responses in rare minnow exposed to 17β-estradiol during different life stages. Fish Physiol Biochem 35, 341–349 (2009). https://doi.org/10.1007/s10695-008-9247-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-008-9247-9

Keywords

  • Biomarker
  • Estradiol
  • Hermaphrodism
  • Sex ratio
  • Vitellogenin