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BioMed Research International
Volume 2014 (2014), Article ID 412619, 12 pages
http://dx.doi.org/10.1155/2014/412619
Research Article

TBT Effects on the Development of Intersex (Ovotestis) in Female Fresh Water Prawn Macrobrachium rosenbergii

1Department of Environmental Biotechnology, Bharathidasan University, Trichy, Tamil Nadu 620 024, India
2CAS in Marine Biology, Faculty of Marine Sciences, Annamalai University, Parangipettai, Tamil Nadu 608 502, India
3Department of Zoology, University of Madras, Guindy Campus, Chennai, Tamil Nadu 600 025, India

Received 11 February 2014; Revised 5 June 2014; Accepted 9 June 2014; Published 10 July 2014

Academic Editor: Sandra Caeiro

Copyright © 2014 Revathi Peranandam et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. G. Vos, E. Dybing, H. A. Greim et al., “Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation,” Critical Reviews in Toxicology, vol. 30, no. 1, pp. 71–133, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Lintelmann, A. Katayama, N. Kurihara, L. Shore, and A. Wenzel, “Endocrine disruptors in the environment: (IUPAC technical report),” Pure and Applied Chemistry, vol. 75, no. 5, pp. 631–681, 2003. View at Google Scholar · View at Scopus
  3. S. Jobling, M. Nolan, C. R. Tyler, G. Brighty, and J. P. Sumpter, “Widespread sexual disruption in wild fish,” Environmental Science and Technology, vol. 32, no. 17, pp. 2498–2506, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. E. Oberdörster and A. O. Cheek, “Gender benders at the beach: endocrine disruption in marine and estuarine organisms,” Environmental Toxicology and Chemistry, vol. 20, no. 1, pp. 23–36, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. P. Revathi, P. Iyapparaj, L. A. Vasanthi, N. Munuswamy, and M. Krishnan, “Impact of TBT on the vitellogenesis and sex hormones in freshwater prawn Macrobrachium rosenbergii (De Man, 1879),” Aquatic Biosystems, vol. 9, no. 1, article 10, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. M. M. Santos, C. C. Ten Hallers-Tjabbes, A. M. Santos, and N. Vieira, “Imposex in Nucella lapillus, a bioindicator for TBT contamination: Re-survey along the Portuguese coast to monitor the effectiveness of EU regulation,” Journal of Sea Research, vol. 48, no. 3, pp. 217–223, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. M. J. Waldock and J. E. Thain, “Shell thickening in Crassostrea gigas: organotin antifouling or sediment induced?” Marine Pollution Bulletin, vol. 14, no. 11, pp. 411–415, 1983. View at Publisher · View at Google Scholar · View at Scopus
  8. R. B. Laughlin, R. Johannesen, W. French, H. Guard, and F. E. Brinckman, “Structure-activity relationships for organotin compounds,” Environmental Toxicology and Chemistry, vol. 4, no. 3, pp. 343–351, 1985. View at Publisher · View at Google Scholar · View at Scopus
  9. P. Iyapparaj, P. Revathi, R. Ramasubburayan et al., “Antifouling activity of the methanolic extract of Syringodium isoetifolium, and its toxicity relative to tributyltin on the ovarian development of brown mussel Perna indica,” Ecotoxicology and Environmental Safety, vol. 89, pp. 231–238, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. P. Revathi and N. Munuswamy, “Effect of tributyltin on the early embryonic development in the freshwater prawn Macrobrachium rosenbergii (De Man),” Chemosphere, vol. 79, no. 9, pp. 922–927, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. P. Revathi, P. Iyapparaj, N. Munuswamy, L. A. Vasanthi, and M. Krishnan, “Bioaccumulation of tributyltin and its impact on spermatogenesis in mud crab Scylla serrata (Forskal),” Turkish Journal of Biology, vol. 37, no. 3, pp. 296–304, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Revathi, P. Iyapparaj, L. A. Vasanthi, N. Munuswamy, and M. Krishnan, “Ultrastructural changes during spermatogenesis, biochemical and hormonal evidences of testicular toxicity caused by TBT in freshwater prawn macrobrachium rosenbergii (De Man, 1879),” Environmental Toxicology, vol. 13, no. 4, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Segner, K. Caroll, M. Fenske et al., “Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project,” Ecotoxicology and Environmental Safety, vol. 54, no. 3, pp. 302–314, 2003. View at Publisher · View at Google Scholar · View at Scopus
  14. BS. Smith, “Sexuality in the American mud and snail, Nassarius obsoletus Say,” Proceedings of the Malacological Society of London, vol. 39, pp. 231–233, 1971. View at Google Scholar
  15. C. Féral, S. LeGall, J. Lever, and H. H. Boer, “The influence of a pollutant factor (tributyltin) on the neuroendocrine mechanism responsible for the occurrence of a penis in the females of Ocenebra erinacea,” J. Lever and H. H. Boer, Eds., pp. 173–175, North Holland Publishing Company, Amsterdam, The Netherlands, 1983. View at Google Scholar
  16. P. Lubet and W. Streiff, “Contrôle neuroendocrine de la reproduction chez les Mollusques,” Journal de Physiologie, vol. 78, no. 6, pp. 537–542, 1982 (French). View at Google Scholar · View at Scopus
  17. C. Bettin, J. Oehlmann, and E. Stroben, “TBT-induced imposex in marine neogastropods is mediated by an increasing androgen level,” Helgoländer Meeresuntersuchungen, vol. 50, no. 3, pp. 299–317, 1997. View at Google Scholar · View at Scopus
  18. J. Nishikawa, S. Mamiya, T. Kanayama, T. Nishikawa, F. Shiraishi, and T. Horiguchi, “Involvement of the retinoid X receptor in the development of imposex caused by organotins in gastropods,” Environmental Science and Technology, vol. 38, no. 23, pp. 6271–6276, 2004. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Matthiessen and Gibbs P. E., “Critical appraisal of the evidence for tributyltin-mediated endocrine disruption in mollusks,” Environmental Toxicology and Chemistry, vol. 17, pp. 37–43, 1998. View at Google Scholar
  20. M. Nolan, S. Jobling, G. Brighty, J. P. Sumpter, and C. R. Tyler, “A histological description of intersexuality in the roach,” Journal of Fish Biology, vol. 58, no. 1, pp. 160–176, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Jobling, N. Beresford, M. Nolan et al., “Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents,” Biology of Reproduction, vol. 66, no. 2, pp. 272–281, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. J. P. Sumpter and S. Jobling, “Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment,” Environmental Health Perspectives, vol. 103, no. 7, pp. 173–178, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Fenske, R. van Aerle, S. Brack, C. R. Tyler, and H. Segner, “Development and validation of a homologous zebrafish (Danio rerio Hamilton-Buchanan) vitellogenin enzyme-linked immunosorbent assay (ELISA) and its application for studies on estrogenic chemicals,” Comparative Biochemistry and Physiology C: Toxicology and Pharmacology, vol. 129, no. 3, pp. 217–232, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Gimeno, A. Gerritsen, T. Bowmer, and H. Komen, “Feminization of male carp,” Nature, vol. 384, no. 6606, pp. 221–222, 1996. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Jobling, D. Sheahan, J. A. Osborne, P. Matthiessen, and J. P. Sumpter, “Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals,” Environmental Toxicology and Chemistry, vol. 15, no. 2, pp. 194–202, 1996. View at Publisher · View at Google Scholar
  26. S. R. Miles-Richardson, V. J. Kramer, S. D. Fitzgerald et al., “Effects of waterborne exposure of 17-estradiol on secondary sex characteristics and gonads of fathead minnows (Pimephales promelas),” Aquatic Toxicology, vol. 47, pp. 129–145, 1999. View at Publisher · View at Google Scholar · View at Scopus
  27. T. L. Metcalfe, C. D. Metcalfe, Y. Kiparissis, A. J. Niimi, C. M. Foran, and W. H. Benson, “Gonadal development and endocrine responses in Japanese medaka (Oryzias latipes) exposed to o,p'-DDT in water or through maternal transfer,” Environmental Toxicology and Chemistry, vol. 19, no. 7, pp. 1893–1900, 2000. View at Google Scholar · View at Scopus
  28. D. E. Hinton, P. C. Baumann, G. R. Gardner et al., Biomarkers: Biochemical, Physiological and Histopathological Markers of Anthropogenic Stress, Lewis Publishers, Boca Ration, Fla, USA, 1992.
  29. C. R. Tyler and E. J. Routledge, “Oestrogenic effects in fish in English rivers with evidence of their causation,” Pure and Applied Chemistry, vol. 70, no. 9, pp. 1795–1804, 1998. View at Publisher · View at Google Scholar · View at Scopus
  30. S. Jobling, D. Casey, T. Rodgers-Gray et al., “Comparative responses of molluscs and fish to environmental estrogens and an estrogenic effluent,” Aquatic Toxicology, vol. 65, no. 2, pp. 205–220, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. G. D. Stentiford and S. W. Feist, “First reported cases of intersex (ovotestis) in the flatfish species dab Limanda limanda: Dogger Bank, North Sea,” Marine Ecology Progress Series, vol. 301, pp. 307–310, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. W. J. Langston, G. R. Burt, and B. S. Chesman, “Feminisation of male clams Scrobicularia plana from estuaries in Southwest UK and its induction by endocrine-disrupting chemicals,” Marine Ecology Progress Series, vol. 333, pp. 173–184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. L. L. Zhang, Z. H. Zuo, Y. X. Chen, Y. Y. Zhao, S. Hu, and C. G. Wang, “Effect of tributyltin on the development of ovary in female cuvier (Sebastiscus marmoratus),” Aquatic Toxicology, vol. 83, no. 3, pp. 174–179, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. A. R. Spurr, “A low-viscosity epoxy resin embedding medium for electron microscopy,” Journal of Ultrasructure Research, vol. 26, no. 1-2, pp. 31–43, 1969. View at Publisher · View at Google Scholar · View at Scopus
  35. B. Tsukimura, J. S. Bender, and C. J. Linder, “Development of an anti-vitellin ELISA for the assessment of reproduction in the ridgeback shrimp, Sicyonia ingentis,” Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology, vol. 127, no. 2, pp. 215–224, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. P. F. Zagalsky, D. F. Cheesman, and H. J. Ceccaldi, “Studies on carotenoid-containing lipoproteins isolated from the eggs and ovaries of certain marine invertebrates,” Comparative Biochemistry and Physiology, vol. 22, no. 3, pp. 851–871, 1967. View at Publisher · View at Google Scholar · View at Scopus
  37. G. P. Oreczyk, B. V. Caldwell, and H. R. Behrman, “Endocrinology,” in Methods of hormone Radioimmunoassay, B. M. Jaffe and H. R. Behrman, Eds., pp. 256–258, Academic press, New York, NY, USA, 1974. View at Google Scholar
  38. D. E. Kime, M. Ebrahimi, K. Nysten et al., “Use of computer assisted sperm analysis (CASA) for monitoring the effects of pollution on sperm quality of fish; application to the effects of heavy metals,” Aquatic Toxicology, vol. 36, no. 3-4, pp. 223–237, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Subramoniam, “Endocrine regulation of egg production in economically important crustaceans,” Current Science, vol. 76, no. 3, pp. 350–360, 1999. View at Google Scholar · View at Scopus
  40. E. M. Rodríguez, L. S. López Greco, and M. Fingerman, “Inhibition of ovarian growth by cadmium in the fiddler crab, Uca pugilator (Decapoda, Ocypodidae),” Ecotoxicology and Environmental Safety, vol. 46, no. 2, pp. 202–206, 2000. View at Publisher · View at Google Scholar · View at Scopus
  41. T. R. Meyers and J. D. Hendricks, “Histopathology,” in Fundamentals of Aquatic Toxicology, G. M. Rand and S. R. Petrocelli, Eds., pp. 283–331, Hemisphere, New York, NY, USA, 1985. View at Google Scholar
  42. A. Sarojini and B. Victor, “Toxicity of mercury on the ovaries of the caridean prawn,” Current Science, vol. 54, pp. 398–400, 1985. View at Google Scholar
  43. L. Shukla, A. Srivastava, D. Merwani, and A. K. Pandey, “Effect of sub-lethal malathion on ovarion histopathology in Sarotherodon mossanbicus,” Comparative Physiology & Ecology, vol. 9, article 12, 1984. View at Google Scholar
  44. P. K. Saxena and M. Garg, “Effect of insecticidal pollution on ovarian recrudescence in the fresh water teleost, Channa punctatus,” Indian Journal of Experimental Biology, vol. 16, no. 6, pp. 690–691, 1978. View at Google Scholar · View at Scopus
  45. L. I. Johnson, E. Casillas, T. K. Collier, B. B. McCain, and U. Varanasi, “Contaminated effects of ovarian development in English sole (Parophrys vetulus) from Puget Sound, Washington,” Canadian Journal of Fisheries and Aquatic Sciences, vol. 45, no. 12, pp. 2133–2146, 1988. View at Publisher · View at Google Scholar · View at Scopus
  46. J. H. McCormick, G. N. Stokes, and R. O. Hermanutz, “Oocyte atresia and reproductive success in fathead minnows (Pimephales promelas) exposed to acidified hardwater environments,” Archives of Environmental Contamination and Toxicology, vol. 18, no. 1-2, pp. 207–214, 1989. View at Publisher · View at Google Scholar · View at Scopus
  47. P. E. Davies and L. S. J. Cook, “Catastrophic macroinvertebrate drift and sublethal effects on brown trout, Salmo trutta, caused by cypermethrin spraying on a Tasmanian stream,” Aquatic Toxicology, vol. 27, no. 3-4, pp. 201–224, 1993. View at Publisher · View at Google Scholar · View at Scopus
  48. D. Farmer, I. R. Hill, and S. J. Maund, “A comparison of the fate and effects of two pyrethroid insecticides (lambda-cyhalothrin and cypermethrin) in pond mesocosms,” Ecotoxicology, vol. 4, no. 4, pp. 219–244, 1995. View at Publisher · View at Google Scholar · View at Scopus
  49. A. N. Giri, D. K. Srivastava, and S. P. Trivedi, “Insecticide basathrin induced histo anatomical insult of ovarian tissue of Indian catfish, Heteropneustes fossilis,” Biological Memoirs, vol. 26, pp. 20–24, 2000. View at Google Scholar
  50. J. Oehlmann, P. Fioroni, E. Stroben, and B. Markert, “Tributyltin (TBT) effects on Ocinebrina aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline,” Science of the Total Environment, vol. 188, no. 2-3, pp. 205–223, 1996. View at Publisher · View at Google Scholar · View at Scopus
  51. B. G. McAllister and D. E. Kime, “Early life exposure to environmental levels of the aromatase inhibitor tributyltin causes masculinisation and irreversible sperm damage in zebrafish (Danio rerio),” Aquatic Toxicology, vol. 65, no. 3, pp. 309–316, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. M. M. Santos, J. Micael, A. P. Carvalho et al., “Estrogens counteract the masculinizing effect of tributyltin in zebrafish,” Comparative Biochemistry and Physiology C: Toxicology and Pharmacology, vol. 142, no. 1-2, pp. 151–155, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. K. Nakayama, Y. Oshima, T. Yamaguchi et al., “Fertilization success and sexual behavior in male medaka, Oryzias latipes, exposed to tributyltin,” Chemosphere, vol. 55, no. 10, pp. 1331–1337, 2004. View at Publisher · View at Google Scholar · View at Scopus
  54. D. E. Kime, Endocrine Distruption in Fish, Kluwer Academic Publishers, Dordrecht, The Netherlands, 1999.
  55. K. Vijayavel and M. P. Balasubramanian, “Fluctuations of biochemical constituents and marker enzymes as a consequence of naphthalene toxicity in the edible estuarine crab Scylla serrata,” Ecotoxicology and Environmental Safety, vol. 63, no. 1, pp. 141–147, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. K. Vijayavel, C. Anbuselvam, M. P. Balasubramanian, V. Deepak, M. Samuel, and S. Gopalakrishnan, “Assessment of biochemical components and enzyme activities in the estuarine crab Scylla tranquebarica from naphthalene contaminated habitants,” Ecotoxicology, vol. 15, no. 5, pp. 469–476, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. K. Vijayavel and M. P. Balasubramanian, “Reproductive dysfunction induced by naphthalene in an estuarine crab Scylla serrata with reference to vitellogenesis,” Ecotoxicology and Environmental Safety, vol. 69, no. 1, pp. 89–94, 2008. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Elumalai, C. Antunes, and L. Guilhermino, “Alterations of reproductive parameters in the crab Carcinus maenas after exposure to metals,” Water, Air, & Soil Pollution, vol. 160, no. 1–4, pp. 245–258, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. J. J. Pereira, J. Ziskowski, R. Mercaldo-Allen, C. Kuropat, D. Luedke, and E. Gould, “Vitellogenin in winter flounder (Pleuronectes americanus) from Long Island Sound and Boston Harbor,” Estuaries, vol. 15, no. 3, pp. 289–297, 1992. View at Publisher · View at Google Scholar · View at Scopus
  60. S. J. Hyllner and C. Haux, “Vitelline envelope protein in teleost fish,” in Proceedings of the 15th International Symposium on the Reproductive Physiology of Fish, F.W. Goetz, Thomas P., and Austin, Eds., vol. 95 of Fish Symposium, pp. 10–12, 1995.
  61. X. T. Chang, T. Kobayashi, H. Kajiura, M. Nakamura, and Y. Nagahama, “Isolation and characterization of the cDNA encoding the tilapia (Oreochromis niloticus) cytochrome P450 aromatase (P450arom): changes in P450arom mRNA, protein and enzyme activity in ovarian follicles during oogenesis,” Journal of Molecular Endocrinology, vol. 18, no. 1, pp. 57–66, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. B. S. Sant'Anna, A. Turra, and F. J. Zara, “Simultaneous activity of male and female gonads in intersex hermit crabs,” Aquatic Biology, vol. 10, no. 3, pp. 201–209, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Shimasaki, T. Kitano, Y. Oshima, S. Inoue, N. Imada, and T. Honjo, “Tributyltin causes masculinization in fish,” Environmental Toxicology and Chemistry, vol. 22, no. 1, pp. 141–144, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. P. Revathi, Studies on the endocrine disruptor and its impact on the reproductive physiology of the freshwater prawn Macrobrachium rosenbergii (De Man) [Thesis], University of Madras, Chennai, India, 2012.