Fish Physiology and Biochemistry

, Volume 40, Issue 5, pp 1495–1507 | Cite as

Structural and functional effects of early exposure to 4-nonylphenol on gonadal development of Nile tilapia (Oreochromis niloticus): b-histological alterations in testes

  • T. El-Sayed Ali
  • S. H. Abdel-Aziz
  • A.-F. M. El-Sayed
  • S. Zeid


The present study investigates the effects of different doses (0, 40, 60, 100 μg/L) of 4-nonylphenol (NP) on testis histology and sperms motility of mature Oreochromis niloticus. A tendency for a dose-dependent reduction in the gonado-somatic index (GSI) in the NP-exposed groups was observed. Histological examination revealed that high doses of NP (60 and 100 μg/L) cause hyperplasia of interlobular connective tissue components coincide with decrease in the size of seminiferous lobules and amount of lumen spermatozoa in comparison with the control and low-dose (40 μg/L)-exposed groups. In addition, within the seminiferous lobules, rupture of spermatogenic cysts, vacuolation and necrosis of primary spermatocytes due to damage of sertoli cells were clearly observed and lead to decrease in advanced spermatogenic cells. The highest dose caused significant decrease in the GSI associated with appearance of testis–ova (intersex) state. The percentage of abnormal sperms increased with increasing the dose of NP reaching to 96 % for those subjected to 100 μg NP/L, while it was only 11 % for the control group specimens. The study indicates that NP has estrogenic potency induced marked alteration in the sexual development including inhibition in testicular growth and deformation in the sperms.


Nonylphenol Oreochromis niloticus Testis histology Sperm motility Testis-ova state 


  1. Beverage MCM, McAndrew BJ (2000) Tilapia biology and exploitation. Fish and fisheries series 25. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  2. 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 59:1479–1487CrossRefGoogle Scholar
  3. Blazquez M, Zanuy S, Carrillo M, Piferrer F (1998) Structural and functional effects of early exposure to estradiol- 17β- and 17α-ethinylestradiol on the gonads of the gonochoristic teleost (Dicentrarchus labrax). Fish Physiol Biochem 18:37–47CrossRefGoogle Scholar
  4. Cardinali M, Maradonna F, Olivotto I, Bortoluzzi G, Mosconi G, Polzonetti-Magni AM (2004) Temporary impairment of reproduction in freshwater teleost exposed to nonylphenol. Reprod Toxicol 18:597–604PubMedCrossRefGoogle Scholar
  5. Cherry N, Labreche F, Collins J, Tulandi T (2001) Occupational exposure to solvents and male infertility. Occup Environ Med 58:635–640PubMedCentralPubMedCrossRefGoogle Scholar
  6. De Rosa M, Zarrilli S, Paesano L, Carbone U, Boggia B, Petretta M, Maisto A, Cimmino F, Puca G, Colao A, Lombardi G (2003) Traffic pollutants affect fertility in men. Hum Reprod 18(5):1055–1061PubMedCrossRefGoogle Scholar
  7. Desbrow C, Routledge EJ, Brighty GC, Sumpter JP, Waldock M (1998) Identification of estrogenic chemicals in STW effluent, 1. Chemical fractionation and in vitro biological screening. Environ Sci Technol 32:1549–1558CrossRefGoogle Scholar
  8. El-Sayed AFM (2006) Tilapia culture. CABI, WallingfordCrossRefGoogle Scholar
  9. Elsayed Ali T (2011) Developmental toxicity of nonylphenol in Zebra fish (Danio rerio) embryos. Indian J Mar Sci 40:509–515Google Scholar
  10. Elsayed Ali T, Legler J (2011) Developmental toxicity of nonylphenol in Zebra fish (Danio rerio) embryos. Indian J Mar Sci 40:509–515Google Scholar
  11. El-Sayed Ali T, Legler J (2010) Overview of the mammalian and environmental toxicity of chlorinated paraffins. In: de Boer J (ed) The Handbook of Environmental Chemistry. vol 10, pp 135–154Google Scholar
  12. Feng M, Chen P, Wei X, Zhang Y, Zhang W, Qi Y (2011) Effect of 4-nonylphenol on the sperm dynamic parameters morphology and fertilization rate of Bufo raddei. Afr J Biotechnol 10:2698–2707CrossRefGoogle Scholar
  13. Filler R (1993) Methods for evaluation of rat epididymal sperm morphology. In: Chapin RE (ed) Methods in toxicology, male reproductive toxicology, vol. 3, (part A). Academic Press Limited, London, pp 334–343Google Scholar
  14. Gautam GJ, Chaube R, Joy KP (2011) 4-Nonylphenol impairs ovarian recrudescence and induces atresia in the cat fish (Heteropneustes fossils). Indian J Sci Technol 4:9–14Google Scholar
  15. Giesy JP, Pierens SL, Snyder EM, Richardson SM, Kramer VJ, Snyder SN, Nichols KM, Villeneuve DA (2000) Effects of 4-Nonylphenol on fecundity biomarkers of estrogenicity in fathead minnow (Pimephales promelas). Environ Toxicol Chem 19:1368–1377CrossRefGoogle Scholar
  16. Harries JE, Runnalls T, Hill E, Harris CA, Maddix S, Sumpter JP, Tyler CR (2000) Development of a reproductive performance test for endocrine disrupting chemicals using pair-breeding fathead minnow (Pimephales promelas). Environ Sci Technol 34:3003–3011CrossRefGoogle Scholar
  17. Hatef A, Alavi SM, Milla S, Kristan J, Golshan M, Fontaine P, Linhart O (2012a) Anti-androgen vinclozolin impairs sperm quality and steroidogenesis in goldfish. Aquat Toxicol 122–123:181–187PubMedCrossRefGoogle Scholar
  18. Hatef A, Alavi SM, Milla S, Abdulfatah A, Fontaine P, Rodina M, Linhart O (2012b) Adverse effects of bisphenol A on reproductive physiology in male goldfish at environmentally relevant concentrations. Ecotoxicol Environ Saf 76:56–62PubMedCrossRefGoogle Scholar
  19. Isobe T, Takada H (2004) Determination of degradation products of alkylphenol polyethoxylates in municipal wastewaters and rivers in Tokyo, Japan. Environ Toxicol Chem 23:599–605PubMedCrossRefGoogle Scholar
  20. Jobling S, Sheahan D, Osborne JA, Matthiessen P, Sumpter JP (1996) Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss). Environ Toxicol Chem 15:194–202CrossRefGoogle Scholar
  21. Jobling S, Beresford N, Nalon M, Rodgers-Gray T, Brighty GC, Sumpter JP, Tyler CR (2002) Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Boil Reprod 66:272–281CrossRefGoogle Scholar
  22. Kammann U, Vobach M, Wosniok W, Schaffer A, Telscher A (2009) Acute toxicity of 353-nonylphenol and its metabolites for zebrafish embryos. Environ Sci Pollut Res 16(2):227–231CrossRefGoogle Scholar
  23. Kinnberg K, Toft G (2003) Effects of estrogenic and antiandrogenic compounds on the testis structure of the adult guppy (Poecilia reticulate). Ecotoxicol Environ Saf 54:16–24PubMedCrossRefGoogle Scholar
  24. Lange A, Yoshinao K, Shinichi M, Yukiko O, Hiroshi U, Tohru K, Toshiaki H, Janice SA, Masaki N, Yuta O, Tomohiro O, Norihisa T, Taisen I, Tyler CR (2011) Comparative responsiveness of test and sentinel fish species to natural and synthetic oestrogens. Indian J Sci Technol 4:9–14Google Scholar
  25. Lee HB, Peart TE, Chan J, Gris G (2004) Occurrence of endocrine-disrupting chemicals in sewage and sludge samples in Toronto, Canada. Water Qual Res J Can 39:57–63Google Scholar
  26. Makynen EA, Kahl MD, Jensen KM, Tietge JE, Wells KL, Van der Kraak G, Ankley GT (2000) Effects of the mammalian antiandrogen vinclozolin on development and reproduction of the fathead minnow (Pimephales promelas). Aquat Toxicol 48:461–475PubMedCrossRefGoogle Scholar
  27. McLaughlin BA, Nelson D, Erecinska M (1998) Toxicity of dipamine to striatal neueons in vitro and potentiation of cell death by a mitochondrial inhibitor. J Neurochem 70:2406–2415PubMedCrossRefGoogle Scholar
  28. McManus JFA, Mowry RW (1964) Staining methods. Histological and histochemical. Harper & Row, New YorkGoogle Scholar
  29. Meier S, Andersen TE, Norberg B, Thorsen A, Taranger GL, Kjesbu OS, Dale R, Morton HC, Klungsøyr J, Svardal A (2007) Effects of alkylphenols on the reproductive system of Atlantic cod (Gadus morhua). Aquat Toxicol 8:207–218CrossRefGoogle Scholar
  30. Miles-Richardson SR, Kramer VJ, Fitzgerald SD, Render JA, Yamini B, Barbee SJ, Giesy JP (1999) Effects of waterborne exposure of 17 b-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas). Aquat Toxicol 47:129–145CrossRefGoogle Scholar
  31. Mitchelmore CL, Rice CP (2006) Correlations of nonylphenol-ethoxylates and nonylphenol with biomarkers of reproductive function in carp (Cyprinus carpio) from the Cuyahoga River. Sci Total Environ 371:391–401PubMedCrossRefGoogle Scholar
  32. Nielsen L, Baatrup E (2006) Quantitative studies on the effects of environmental estrogens on the testis of the guppy, Poecilia reticulate. Aquat Toxicol 80:140–148PubMedCrossRefGoogle Scholar
  33. Panter GH, Thompson RS, Sumpter JP (1998) Adverse reproductive effects in male fathead minnows (Pimephales promelas) exposed to environmentally relevant concentrations of the natural estrogens, estradiol and estrone. Aquat Toxicol 42:243–253CrossRefGoogle Scholar
  34. Partridge C, Boettcher A, Jones AG (2010) Short-term exposure to a synthetic estrogen disrupts mating dynamics in a pipefish. Horm Behav 58(5):800–807PubMedCrossRefGoogle Scholar
  35. Sayed AH, Mahmoud UM, Mekkawy IAA (2012) Reproductive biomarkers to identify endocrine disruption in Clarias gariepinus exposed to 4-nonylphenol. Ecotoxicol Environ Saf 78:310–319CrossRefGoogle Scholar
  36. Snedecor GW, Cochran WG (1989) Statistical methods, vol 8. Iowa State University Press, AmesGoogle Scholar
  37. Stachel B, Jantzen E, Knoth W, Kruger F, Lepom P, Oetken A, Reincke H, Sawal G, Schwartz R, Uhlig S (2005) The Elbe flood in August 2002-organic contaminants in sediment samples taken after the flood event. J. Environ Sci Health A 40:265–287CrossRefGoogle Scholar
  38. Swan SH, Kruse RL, Liu F, Barr DB, Drobnis EZ, Redmon JB (2003) Semen quality in relation to biomarkers of pesticide exposure. Environ Health Perspect 111:1478–1484PubMedCentralPubMedCrossRefGoogle Scholar
  39. Trudeau VL, Peter RE, Soly BD (1991) Testosterone and estradiol potentiate the serum gonadotropin response to gonadotropin response to releasing hormone in gold fish. Biol Reprod 48:951–960CrossRefGoogle Scholar
  40. Vander Kraak G, Zacharewski T, Jan, D, Sanders B, Gooch J (1998) Comparative endocrinology and mechanisms of endocrine modulation in fish and wildlife. In: Kendall RJ, Dickerson RL, Suk WA, Giesy JP (eds) Principles and processes for evaluating endocrine disruption in wildlife, pp 97–119Google Scholar
  41. Yutaka H, Carlos AS, Shinya H (2007) Assessment of short-term exposure to nonylphenol in Japanese medaka using sperm velocity and frequency of motile sperm. Arch Environ Contam Toxicol 53:406–410CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • T. El-Sayed Ali
    • 1
    • 2
  • S. H. Abdel-Aziz
    • 1
  • A.-F. M. El-Sayed
    • 1
  • S. Zeid
    • 1
  1. 1.Oceanography Department, Faculty of ScienceAlexandria UniversityAlexandriaEgypt
  2. 2.College of Sciences and Humanity StudiesSalman bin Abdul-Aziz UniversityAlkharjKingdom of Saudi Arabia

Personalised recommendations