Effect of Tributyltin Chloride on Survival, Growth and Reproduction in Zebra Fish Danio rerio

  • Balasubramani, A. (School of Biological Sciences, Madurai Kamaraj University) ;
  • Pandian, T.J. (School of Biological Sciences, Madurai Kamaraj University)
  • Published : 2008.08.25

Abstract

Tributyltin chloride(TBTCl) was administered through discrete immersion(2 hr each) from the $18^{th}-25^{th}$ day after hatching(dph). At the doses of 1, 2, 4 and 8 ${\mu}g/L$, the immersion at 2 ${\mu}g/L$ ensured 93% masculinization and the highest survival of 75% after the treatment. TBTCl acted as a growth suppressant and the magnitude of its suppression was stronger in females. During the 300 day experiment, it postponed sexual maturity of females from 120$^{th}$ dph in the control to 240$^{th}$ dph in the females treated at 8 ${\mu}g/L$. It reduced spawning frequency(22-3 times) and cumulative fecundity(1,632-19 eggs) by reducing the number of vitellogenic eggs. In the treated males too, it reduced sperm motility(100-68 sec); consequently, fertilizability of the sperm cells drawn from these males was also reduced from 88 to 43%. Progeny testing showed that the cross between males treated at>2 ${\mu}g/L$ and normal females generated the presumed 'homogametic' males. Both the treated 'homogametic' and 'heterogametic' males could induce the females to spawn fewer eggs than that of the normal males. A normal female somehow deducted the differences between the control, treated and sex reversed males; it preferred a normal male over a treated one, and a treated one over the sex reversed male.

Keywords

References

  1. Alzieu, C., 2000. Impact of tributyltin on marine invertebrates. Ecotoxicology, 9, 71-76 https://doi.org/10.1023/A:1008968229409
  2. Bayley, M., J.R. Nielsen and E. Baatrup, 1999. Guppy sexual behavior as an effect biomarker of estrogen mimics. Ecotoxicol. Environ. Saf., 43, 68-73 https://doi.org/10.1006/eesa.1999.1766
  3. Billard, R. and M.P. Cosson, 1992. Some problems related to the assessment of sperm motility in freshwater fish. J. Exp. Zool., 261, 122-131 https://doi.org/10.1002/jez.1402610203
  4. Bloom, H.D. and A. Perlmutter, 1977. A sexual aggregating pheromone system in the zebrafish, Brachydanio rerio (Hamilton-Buchanan). J. Exp. Zool., 199, 215-226 https://doi.org/10.1002/jez.1401990206
  5. Darrow, K.O. and W.A. Harris, 2004. Characterization and development of courtship in zebrafish, Danio rerio. Zebrafish, 1, 40-45 https://doi.org/10.1089/154585404774101662
  6. David, C.J. and T.J. Pandian, 2006. Cadaveric sperm induces intergeneric androgenesis in the fish, Hemigrammus caudovittatus. Theriogenology, 65, 1048-1070 https://doi.org/10.1016/j.theriogenology.2005.07.014
  7. Dimitriou, P., J.C. Catharios, H. Miliou, 2003. Acute toxicity effects of tributyltin chloride and triphenyltin chloride on gilthead seabream, Sparus aurata L. embryos. Ecotoxicol. Environ. Saf., 54, 30-35 https://doi.org/10.1016/S0147-6513(02)00008-8
  8. Dong, W, W. Muramoto, Y. Nagai, K. Takehana, J.J. Stageman, H. Teraoka and T. Hiraga, 2006. Retinal neuronal cell is a toxicological target of tributyltin in developing zebrafish. J. Vet. Med. Sci., 68, 573-579 https://doi.org/10.1292/jvms.68.573
  9. Fent, K., 1991. Bioconcentration and elimination of tributyltin chloride by embryos and larvae of minnow Phoxinus phoxinus. Aquat. Toxicol., 20, 147-158 https://doi.org/10.1016/0166-445X(91)90013-Y
  10. George, T., T.J. Pandian, and S. Kavumpurath, 1994. Inviability of YY zygotes of the fighting fish, Betta splendens. Isr. J. Aquacult.-Bamidgeh, 46, 3-8
  11. George, T. and T.J. Pandian, 1995. Production of ZZ females in the female-heterogametic black molly, Poecilia sphenops, by endocrine sex reversal and progeny testing. Aquaculture, 136, 81-90 https://doi.org/10.1016/0044-8486(95)01035-1
  12. Gormley, K.L. and K.L. Teather, 2003. Developmental, behavioural, and reproductive effects experienced by Japanese medaka (Oryzias latipes) in response to short-term exposure to endosulfan. Ecotoxicol. Environ. Saf., 54: 330-338 https://doi.org/10.1016/S0147-6513(02)00005-2
  13. Greco, L., E. Capri and T. Rustad, 2007. Biochemical responses in Salmo salar muscle following exposure to ethynylestradiol and tributyltin. Chemosphere, 68, 564-571 https://doi.org/10.1016/j.chemosphere.2006.12.033
  14. Harino, H., M. Fukushima, Y. Yamamoto, S. Kawai and N. Miyazaki, 1998. Contamination of butyltin and phenyltin compounds in the marine environment of Otsuchi Bay, Japan. Environ. Pollut., 101, 209-214 https://doi.org/10.1016/S0269-7491(98)00047-5
  15. Haubruge, E., F. Petit, M.J.G. Gage, 2000. Reduced sperm counts in guppies (Poecilia reticulata) following exposure to low levels of tributyltin and bisphenol A. Proc. R. Soc. Lond., 267 B, 2333-2337
  16. Horiguchi, T., N. Takiguchi, H.S. Cho, M. Kojima, M. Kaya, H. Shiraishi, M. Morita, H. Hirose and M. Shimizu, 2000. Ovotestis and disturbed reproductive cycle in the giant abalone, Haliotis madaka: possible linkage with organotin contamination in a site of population decline. Mar. Environ. Res., 50, 223-229 https://doi.org/10.1016/S0141-1136(00)00071-4
  17. Hunter, G.A., I.I. Solar, I. J. Baker, and E.M. Donaldson, 1986. Feminization of coho salmon (Oncorhynchus kisutch) and chinook salmon (Oncorhynchus tshawytscha) by immersion of alevins in a solution of estradiol-17$\alpha$. Aquaculture, 53, 295-302 https://doi.org/10.1016/0044-8486(86)90360-1
  18. Kavumpurath, S. and T.J. Pandian, 1992. Production of YY male in the guppy Poecilia reticulata by endocrine sex reversal and progeny testing. Asian Fish. Sci., 5, 265-276
  19. Manning, C.S., T.F. Lytle, W.W. Walker and J. S. Lytle, 1999. Life-cycle toxicity of bis (tributyltin) oxide to the sheepshead minnow (Cyprinodon variegates). Arch. Environ. Contam. Toxicol., 37, 258-266 https://doi.org/10.1007/s002449900513
  20. McAllister, B.G. and D.E. Kime, 2003. Early life exposure to environmental levels of the aromatase inhibitor tributyltin causes masculinization and irreversible sperm damage in zebrafish (Danio rerio). Aquat. Toxicol., 65, 309-316 https://doi.org/10.1016/S0166-445X(03)00154-1
  21. Nakayama, K., Y. Oshima, T. Yamaguchi, Y. Tsuruda, I.J. Kang, M. Kobayashi, N. Imada and T. Honjo, 2004. Fertilization success and sexual behaviour in male medaka, Oryzias latipes, exposed to tributyltin. Chemosphere, 55, 1331-1337 https://doi.org/10.1016/j.chemosphere.2003.11.050
  22. Nakayama, K., Y. Oshima, K. Nagafuchi, T. Hano, Y. Shimasaki and T. Honjo, 2005. Early-life stage toxicity in offspring from exposed parent medaka, Oryzias latipes, to mixtures of tributyltin and polychlorinated biphenyls. Environ. Toxicol. Chem., 24, 591-596 https://doi.org/10.1897/04-157R.1
  23. Nirmala, K., Y. Oshima, R. Lee, N. Imada, T. Honjo, and K. Kobayashi, 1999. Transgenerational toxicity of tributyltin and its combined effects with polychlorinated biphenyls on reproductive processes in Japanese medaka (Oryzias latipes). Environ. Toxicol. Chem., 18, 717-721 https://doi.org/10.1897/1551-5028(1999)018<0717:TTOTAI>2.3.CO;2
  24. Nash, J.P., D.E. Kime, L.T.M. Van der Ven, P.W. Wester, F. Brion, G. Maack, P. Stahlschmidt-Allner, and C.R. Tyler, 2004. Longterm exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Persp., 112, 1725-1733 https://doi.org/10.1289/ehp.7209
  25. Pandian, T.J., S.G. Sheela, 1995. Hormonal induction of sex reversal in fish. Aquaculture, 138, 1-22 https://doi.org/10.1016/0044-8486(95)01075-0
  26. Pandian, T.J., S. Kirankumar, 2003. Recent advances in hormonal induction of sex-reversal in fish. J. Applied Aquacult., 13, 203-230
  27. Petersen, G.I., L. Norrgren, H. Holbech, A. Lundgren, and S. Koivisto, 2001. Suitability of zebrafish as test organism for detection of endocrine disrupting chemicals. Final Manuscript for the Temanord Serie, 5.12.2001 Sweden
  28. Piver, W.T., 1973. Organotin compounds: industrial applications and biological investigation. Environ. Health Persp., 4, 61-79 https://doi.org/10.2307/3428183
  29. Qun-Fang, Z., J. Gui-Bin, L. Ji-Yan, 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 https://doi.org/10.1007/s00244-001-0014-5
  30. Santos, M.M., J. Micael, A.P. Carvalho, R. Morabito, P. Booy, P. Massanisso, M. Lamoree and M.A. Reis-Henriques, 2006. Estrogens counteract the masculinizing effect of tributyltin in zebrafish. Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 142, 151-155 https://doi.org/10.1016/j.cbpc.2005.11.014
  31. Sastry, K.V. and A.A. Siddiqui, 1982. Effect of endosulfan and quinalphos on intestinal absorption of glucose in the freshwater murrel, Channa punctatus. Toxic. Lett., 12, 289-293 https://doi.org/10.1016/0378-4274(82)90253-3
  32. Schmidt, K., G.B.O. Staaks, S. Pflugmacher and C.E.W. Steinberg, 2005. Impact of PCB mixture (Aroclor 1254) and TBT and a mixture of both on swimming behavior, body growth and enzymatic biotransformation activities (GST) of young carp (Cyprinus carpio). Aquat. Toxicol., 71, 49-59 https://doi.org/10.1016/j.aquatox.2004.10.012
  33. Shim, W.J., J.K. Jeon, J.R. Oh, N.S. Kim and S.H. Lee, 2002. Accumulation of tributyltin in the blood of fish: Its application for monitoring in the marine environment. Environ. Toxicol. Chem., 21, 1451-1455 https://doi.org/10.1897/1551-5028(2002)021<1451:AOTITB>2.0.CO;2
  34. Shimasaki, Y., T. Kitano, Y. Oshima, S. Inoue, N. Imada and T. Honjo, 2003. Tributyltin causes masculinization in fish. Environ. Toxicol. Chem., 22, 141-144 https://doi.org/10.1897/1551-5028(2003)022<0141:TCMIF>2.0.CO;2
  35. Shimasaki, Y., Y. Oshima, S. Inoue, Y. Inoue, I.J. Kang, K. Nakayama, H. Imoto and T. Honjo, 2006. Effect of tributyltin on reproduction in Japanese whiting, Sillago japonica. Mar. Environ. Res. 62 Suppl., S245-248 https://doi.org/10.1016/j.marenvres.2006.04.030
  36. Short, J.W., F.P. Thrower, 1986. Accumulation of butyltins in muscle tissue of Chinook salmon reared in sea pens treated with tri-n-butyltin. Mar. Poll. Bull., 17, 542-545 https://doi.org/10.1016/0025-326X(86)90566-7
  37. Suzuki,T., R. Matsuda and Y. Saito, 1992. Molecular species of tri-n-butyltin compounds in marine products. J. Agric. Food Chem., 40, 1437-1443 https://doi.org/10.1021/jf00020a030
  38. Traut, W., H. Winking, 2001. Meiotic chromosomes and stages of sex chromosomes evolution in fish: zebrafish, platyfish and guppy. Chromos. Res., 9, 659-672 https://doi.org/10.1023/A:1012956324417
  39. Uchida, D., M. Yamashita, T. Kitano and T. Iguchi, 2002. Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. J. Exp. Biol., 205, 711-718
  40. Yambe, H., M. Shindo and F. Yamazaki, 1999. A releaser pheromone that attracts males in the urine of mature female masu salmon. J. Fish Biol., 55, 158-171 https://doi.org/10.1111/j.1095-8649.1999.tb00665.x
  41. Zheng, R., C. Wang, Y. Zhao, Z. Zuo and Y. Chen, 2005. Effect of tributyltin, benzo(a)pyrene and their mixture exposure on the sex hormone levels in gonads of cuvier (Sebastiscus marmoratus). Environ. Toxicol. Pharmacol., 20, 361-367 https://doi.org/10.1016/j.etap.2005.03.005