Induction of Intersex and Masculinization of the Equilateral Venus, Gomphina veneriformis (Bivalvia: Veneridae) by Zinc

  • Ju, Sun-Mi (Department of Aqualife Medicine, Chonnam National University) ;
  • Park, Jung-Jun (Marine Environment Research Team, NFRDI) ;
  • Lee, Jung-Sick (Department of Aqualife Medicine, Chonnam National University)
  • Published : 2009.09.30

Abstract

This study aims to find out the effect of heavy metals, as is the case of EDCs (endocrine disrupting chemicals), on reproductive endocrine disruption of aquatic animals. In the present experiment zinc, which is a heavy metal well known for its androgenous activity, was used. The experimental period was 24 weeks, starting in November during the inactive stage of the clam's reproductive cycle. The experimental groups were composed of one control condition and three zinc exposure conditions (0.64, 1.07, and 1.79 mg/L). The sex ratio (F:M) was 1:1.06 in the control group and 1:1.70 in all the exposed group, illustrating the tendency for higher proportion of males with increases in zinc concentration. Gonad maturity was higher in 1.07, and 1.79 mg/L groups compared to the control group, with higher maturity observed in males than females. Intersex individuals made up 24.7% of the exposed group, while females exhibited a higher ratio than the males with increasing zinc concentration. The results of this study indicate that zinc functions as an androgenic effector on the reproduction of Gomphina veneriformis.

Keywords

References

  1. Barbeau C, Bougie R, and Cote IE (1981) Temporal and spatial variations of mercury, lead, zinc, and copper in sediments of the Saguenay fjord. Can J Earth Sci 18: 1065-1074 https://doi.org/10.1139/e81-102
  2. Bedwal RS and Bahuguna A (1994) Zinc, copper and selenium in reproduction. Experientia 50(7): 626-640 https://doi.org/10.1007/BF01952862
  3. Blaise C, Pellerin-Massicote J, and Hansen P-D (1996) Molluscan shellfish biomarker study of the Saguenay fjord, Quebec, Canada. In: Fourth European Conference on Ecotoxicology and Environmental Safety, Metz, France, Abstract C-41
  4. Bortone SA and Davis WP (1994) Fish intersexuality as indicator of environmental stress: Monitoring fish reproductive systems can serve to alert humans to potential harm. Bioscience 44:165-172 https://doi.org/10.2307/1312253
  5. Byrne PA and O'Halloranan J (2001) The role of bivalve molluscs as tools in estuarine sediment toxicity testing: a review. Hydrobiologia 465: 209-217 https://doi.org/10.1023/A:1014584607501
  6. Chesman BS and Langston WJ (2006) Intersex in the clam Scrobicularia plana: a sign of endocrine disruption in estuaries? Biol Lett 2: 420-422 https://doi.org/10.1098/rsbl.2006.0482
  7. Dave G, Damagaard B, Grande M, Martelin IE, Rosander B, and Viktor T (1987) Ring test of an embryo-larval toxicity test with zebrafish, Brachydanio rerio using chromium and zinc as toxicants. Environ Toxicol Chem 6: 61-71 https://doi.org/10.1002/etc.5620060108
  8. Drysdale DT and Bortone SA (1989) Laboratory induction of intersexuality in the mosquitofish, Gambusia affinis, using paper mill effluent. Bull Environ Contam Toxicol 43: 611-617 https://doi.org/10.1007/BF01701943
  9. Eversole AG (1997) Gametogenesis of Mercenaria mercenaria, M campechiensis and their hybrids. Nautilus 110: 107-110
  10. Gagne F, Blaise C, Pellerin J, Pelletier E, Douville M, GauthierClerc S, and Viglino L (2003) Sex alteration in soft-shell clams (Mya arenaria) in an intertidal zone of the Saint Lawrence river (Quebec, Canada). Comp Biochem Physiol C 134: 189-198 https://doi.org/10.1016/S1096-4959(02)00250-6
  11. Gauthier-Clerc S, Pellerin J, Blaise C, and Gagne F (2002) Delayed gametogenesis of Mya arenaria in the Saguenay fjord (Canada): a consequence of endocrine disruptors? Comp Biochem Physiol C 131: 457-467 https://doi.org/10.1016/S1095-6433(01)00485-8
  12. Gibbs PE and Byrne PA (1986) Reproductive failure in populations of the dog-whelk, Nucella lapillus, caused by imposex induced by tributyltin from antifouling paints. J Mar Bioi Assoc UK 66: 767-777 https://doi.org/10.1017/S0025315400048414
  13. Gray MA and Metcalfe CD (1997) Induction of testis-ova in Japanese medaka Oryzias latipes exposed to p-nonylphenol. Environ Toxicol Chem 16: 1082-1086 https://doi.org/10.1002/etc.5620160531
  14. Horiguchi T, Shiraishi H, Shimizu M, and Morita M (1994) Imposex and organotin compounds in Thais clavigera and T bronniin in Japan. J Mar Bioi Assoc UK 74: 651-669 https://doi.org/10.1017/S002531540004772X
  15. Horiguchi T, TakiguchiN, Cho HS, Kojima M, Kaya M, Shiraishi H, Morita M, Hirose H, and ShimizuM (2000) Ovo-testis 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
  16. Kahng SH, Je JG,Oh JR, Shim WJ, and Shim JH (1996) Imposex of Thais clavigera and T luteostoma (Muricidae) as an evidence of organotin pollution in Chinhae bay. Korean J Malacol 12: 123-131
  17. Lee JS and Park JJ (2007) Risk assessment of nonylphenol using sex ratio, sexual maturation, intersex and lipofuscin accumulation of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae).J Kor Fish Soc 40: 16-23 https://doi.org/10.5657/kfas.2007.40.1.016
  18. Mackie GL (1984) Bivalves. In: Tompa AS, Verdonk NH, and Van den Biggelaar JAM (eds), The Mollusca Vol.7. Reproduction, Academic Press, New York,pp 351-418
  19. Martel L, Gagnon MJ, Masse' R, Leclerc A, and Tremblay L (1986) Polycyclic aromatic hydrocarbons in sediments from the Saguenay Fjord, Canada. Bull Environ Contam Toxicol 37: 133-140 https://doi.org/10.1007/BF01607740
  20. Matozzo V and Marin MG (2005) Can 4-nonylphenol induce vitellogenin-like proteins in the clam Tapes philippinarum ? Environ Res 97: 43-49 https://doi.org/10.1016/j.envres.2004.03.002
  21. Mauri M, Orlando E, Negro M, and Regoli F (1990) Heavy etals in the Antarctic scallop, Adamussium colbecki. Mar Ecol Prog Ser 67: 27-33 https://doi.org/10.3354/meps067027
  22. McConnell MA and Jarrel RC (1995) The estuarine clam, Rangia cuneata (Rray) as a biomonitor of heavy metals under laboratory and field conditions. Amer Malacol Bull 11: 191-201
  23. Morcillo Y and Porte C (2000) Evidence of endocrine disruption in clams Ruditapes decussate transplanted to a tributyltinpolluted environment. Environ Pollut 107: 47-52 https://doi.org/10.1016/S0269-7491(99)00133-5
  24. Munkittrick KR and VanDer Kraak G (2000) Appropriate uses of physiological techniques for endocrine studies. In: Henshel DS, Black MC, and Harrass MC (eds), Environmental Toxicology and Risk Assessment: Standardization of Biomarkers for Endocrine Disruption and Environmental Assessment Vol.8,ASTM, West Conshohocken, pp 95-118
  25. Olsson P-E (1998) Chapter 4. Disorders associated with heavy metal pollution. In: Leatherland JF, and Woo PTK (eds), Fish Diseases and Disorders Vol. 2. Non-infectious Disorders, CABI Publishing, New York,pp 105-131
  26. Park JJ, Lee JY, Lee JS, and Chang YJ (2003) Gonadal development and gametogenic cycle of the equilateral venus, Gomphina veneriformis (Bivalvia: Veneridae).J Kor Fish Soc 36: 352-357 https://doi.org/10.5657/kfas.2003.36.4.352
  27. Quinn B, Gagne F, Blaise C, Costello MJ, Wilson JG, and Mothersill C (2006) Evaluation of the lethal the sub-lethal toxicity and potential endocrine disrupting effect of nonylphenol on the zebra mussel (Dreissena polymorpha). Comp Biochem Physiol C 142: 118-127 https://doi.org/10.1016/j.cbpc.2005.11.004
  28. Quinn B, Gagne F, Costello M, McKenzie C, Wilson J, and Mothersill C (2004) The endocrine disrupting effect of municipal effluent on the zebra mussel (Dreissena polymorpha). Aquat Toxicol 66: 297-292 https://doi.org/10.1016/j.aquatox.2003.10.007
  29. Rainbow PS (1993) The significance of trace metal concentration in marine invertebrates. In: Dallinger R and Rainbow PS (eds), Ecotoxicology of Metals in Invertebrates, Lewis Publishers, Boca Raton, FL, pp 1-461
  30. Siah A, Pellerin J, Amiard JC, Pelletier E, and Viglino L (2003) Delayed gametogenesis and progesterone levels in soft-shell clams (Mya arenaria) in relation to in situ contamination to organotins and heavy metals in the St. Lawrence River (Canada). Comp Biochem Physiol C 135: 145-156 https://doi.org/10.1016/S1532-0456(03)00085-1
  31. Skidmore JF (1970) Respiration and osmoregulation in rainbow trout with gills damaged by zinc sulfate. J Exp Biol 52: 481-494
  32. Stromgren T and Nielsen MV (1991) Spawning frequency, growth and mortality of Mytilus edulis larvae, exposed to copper and diesel oil. Aquat Toxicol 21: 171-180 https://doi.org/10.1016/0166-445X(91)90071-G
  33. Timmermans BMH, Hummel H, and Bogaards RH (1996) The effect of polluted sediment on the gonadal development and embryogenesis of bivalves. Sci Total Environ 187: 231-236 https://doi.org/10.1016/0048-9697(96)05145-5
  34. Viarengo A (1985) Biochemical effects of trace metals. Mar Pollut Bull 16: 153-158 https://doi.org/10.1016/0025-326X(85)90006-2
  35. Yoo J-S (1988) Korean shells in color. Iljisa Publishing Co, Seoul, pp 1-196