Environmental Monitoring and Assessment

, Volume 186, Issue 3, pp 1453–1463 | Cite as

Accumulation of endocrine disrupting chemicals (EDCs) in the polychaete Paraprionospio sp. from the Yodo River mouth, Osaka Bay, Japan

  • Mohd Yusoff Nurulnadia
  • Jiro Koyama
  • Seiichi Uno
  • Asami Kito
  • Emiko Kokushi
  • Eugene Tan Bacolod
  • Kazuki Ito
  • Yasutaka Chuman


This study presents the levels of endocrine disrupting chemicals (EDCs) accumulated by Paraprionospio sp. from the Yodo River mouth, Osaka Bay. Since high concentrations of nonylphenol (NP), bisphenol A (BP), octylphenol (OP), 17β-estradiol (E2), and estrone (E1) have been measured in sediment from Osaka Bay, some bioaccumulation could be expected particularly in benthic animals. EDCs were analysed in Paraprionospio sp., a dominant benthic species in Osaka Bay. The results showed that Paraprionospio sp. had accumulated varying concentrations (wet weight; w.w.) of NP at 1,460–4,410 ng/g; BP at 22.5–39.6 ng/g; OP at 18.9–45.4 ng/g; E2 at 0.89–4.35 ng/g; and E1 at 0.06–2.50 ng/g. Accumulation of NP and OP were highest among the samples gathered in summer (July 2008), while concentrations of BP, E2, and E1 did not much differs within 3 years. EDC levels in Paraprionospio sp. were apparently greater than those in sediments showing bioaccumulation.


Bioaccumulation EDCs Paraprionospio sp. Osaka Bay 



The present study was partly funded by the EXTEND 2010 Program, Ministry of Environment, Japan. The authors would like to express their gratitude to Associate Prof. Gilma Tayo of College of Fisheries and Ocean Sciences, University of the Philippines Visayas, for the kind comments and recommendations.


  1. Ahel, M., & Giger, W. (1993). Partitioning of alkylphenols and alkylphenol polyethoxylates between water and organic solvents. Chemosphere, 26, 1471–1478.CrossRefGoogle Scholar
  2. Association for New Social Infrastructure of Osaka Bay (Ed.). (1996). Communication tool for sustainable development. Osaka: Institute of Coastal Environment. in Japanese.Google Scholar
  3. Basheer, C., Hian, K. L., & Koh, S. T. (2004). Endocrine disrupting alkylphenols and bisphenol-A in coastal waters and supermarket seafood from Singapore. Baseline/Marine Pollution Bulletin, 48, 1145–1167.CrossRefGoogle Scholar
  4. Campbell, C. G., Borglin, S. E., Green, F. B., Grayson, A., Wozei, E., & Stringfellow, W. T. (2006). Biologically directed environmental monitoring, fate, and transport of estrogenic endocrine disrupting compounds in water: a review. Chemosphere, 65, 1265–1280.CrossRefGoogle Scholar
  5. deFur, P. L., Crane, M., Ingersoll, C., & Tattersfield, L. (eds). (1999). Endocrine disruption in invertebrates: Endocrinology, testing, and assessment. In Proceedings of the Workshops on Endocrine Disruption in Invertebrates, 12–15 Dec. 1998, Noordwijkerhout, The Netherlands. Pensacola, FL: SETAC Press.Google Scholar
  6. Fauchald, K., & Jumars, P. A. (1979). The diet of worms: a study of polychaete feeding guilds. Oceanography and Marine Biology. Annual Review, 17, 193–284.Google Scholar
  7. Ferrara, F., Fabietti, F., Delise, M., Bocca, A. P., & Funari, E. (2001). Alkylphenolic compounds in edible molluscs of the Adriatic Sea, Italy. Environmental Science and Technology, 35, 3109–3112.CrossRefGoogle Scholar
  8. Ferrara, F., Fabietti, F., Delise, M., & Funari, E. (2005). Alkylphenols and alkylphenol ethoxylates contamination of crustaceans and fishes from the Adriatic Sea (Italy). Chemosphere, 59, 1145–1150.CrossRefGoogle Scholar
  9. Ferrara, F., Ademollo, N., Delise, M., Fabietti, F., & Funari, E. (2008). Alkylphenols and their ethoxylates in seafood from the Tyrrhenian Sea. Chemosphere, 72, 1279–1285.CrossRefGoogle Scholar
  10. Fernandes, M., Shareef, A., Karkkainen, M., & Kookana, R. (2008). The occurrence of endocrine disrupting chemicals and triclosan in sediments of Banker Inlet, South Australia. A report prepared for the Adelaide and Mount Lofty Ranges Natural Resources Management Board. SARDI Publication Number F2008/001026-1 (p. 11). Adelaide: South Australian Research & Development Institute (Aquatic Sciences).Google Scholar
  11. Folmar, L. C., Denslow, N. D., Kroll, K., Orlando, E. F., Enblom, J., Marcino, J., et al. (2001). Altered serum sex steroids and vitellogenin induction in walleye (Stizostedion vitreum) collected near a metropolitan sewage treatment plant. Archives of Environmental Contamination and Toxicology, 40, 392–398.CrossRefGoogle Scholar
  12. Hashimoto, S., Horiuchi, A., Yoshimoto, T., Nakao, M., Omura, H., Kato, Y., et al. (2005). Horizontal and vertical distribution of estrogenic activities in sediments and waters from Tokyo Bay, Japan. Archives of Environmental Contamination and Toxicology, 48(2), 209–216.CrossRefGoogle Scholar
  13. Holmer, M., & Kristensen, E. (1996). Seasonality of sulfate reduction and pore water solutes in a marine fish farm sediment: the importance of temperature and sedimentary organic matter. Biogeochemistry, 32, 15–39.CrossRefGoogle Scholar
  14. Hosono, T., Su, C., Okamura, K., & Taniguchi, M. (2010). Historical record of heavy metal pollution deduced by lead isotope ratios in core sediments from the Osaka Bay, Japan. Journal of Geochemical Exploration, 107, 1–8.CrossRefGoogle Scholar
  15. Hu, J., Jin, F., Wan, Y., Yang, M., An, L., & Tao, S. (2005). Trophodynamic behavior of 4-nonylphenol and nonylphenol polyethoxylate in a marine aquatic food web from Bohai Bay, North China: Comparison to DDTs. Environmental Science and Toxicology, 39, 4801–4807.Google Scholar
  16. Hubas, C., Artigas, L. F., & Davoult, D. (2007). Role of bacterial community in the annual benthic metabolism of two contrasted temperate intertidal sites (Roscoff Aber Bay, France). Marine Ecology Progress Series, 344, 39–48.CrossRefGoogle Scholar
  17. Imai, S., Koyama, J., & Fujii, K. (2005). Effects of 17β-estradiol on the reproduction of Java medaka (Oryzias javanicus), a new test fish species. Marine Pollution Bulletin, 51, 708–714.CrossRefGoogle Scholar
  18. Imai, S., Koyama, J., & Fujii, K. (2007). Effects of estrone on full life cycle of Java medaka, a new marine test fish. Environmental Toxicology & Chemistry, 26, 726–731.CrossRefGoogle Scholar
  19. Isobe, T., Nishiyama, H., Nakashima, A., & Takada, H. (2001). Distribution and behavior of nonylphenol, octylphenol, and nonylphenol monoethoxylate in Tokyo metropolitan area: Their association with aquatic particles and sedimentary distributions. Environmental Science and Technology, 35, 1041–1049.CrossRefGoogle Scholar
  20. Isobe, T., Serizawa, S., Horiguchi, T., Shibata, Y., Managaki, S., Takada, H., et al. (2006). Horizontal distribution of steroid estrogens in surface sediments in Tokyo Bay. Environmental Pollution, 144, 632–638.CrossRefGoogle Scholar
  21. Japanese Ministry of Environment. (2002). The report of endocrine disrupting chemicals in the water environment (p. 35). Tokyo: Japanese Ministry of Environment.Google Scholar
  22. Jobling, S., Sumpter, J. P., Sheahan, D., Osborne, J. A., & Matthiessen, P. (1996). Inhibition of testicular growth in rainbow trout (Oncorhyncus mykiss) exposed to estrogenic alkylphenolic chemicals. Environmental Toxicology and Chemistry, 15(2), 194–202.Google Scholar
  23. Jurgens, M. D., Holthaus, K. I. E., Johnson, A. C., Smith, J. J. L., Hetheridge, M., & Williams, R. J. (2002). The potential for estradiol and ethinylestradiol degradation in English rivers. Environmental Toxicology & Chemistry, 21, 480–488.CrossRefGoogle Scholar
  24. Kawahata, H., Ohta, H., Inoue, M., & Suzuki, A. (2004). Endocrine disrupter nonylphenol and bisphenol A contamination in Okinawa and Ishigaki Islands, Japan within coral reefs and adjacent river mouths. Chemosphere, 55, 1519–1527.CrossRefGoogle Scholar
  25. Koyama, J., Kitoh, A., Nakai, M., Kohno, K., Tanaka, H., & Uno, S. (2013). Relative contribution of endocrine-disrupting chemicals to the estrogenic potency of marine sediments of Osaka Bay, Japan. Water, Air, and Soil Pollution, 224, 1570. doi: 10.1007/s11270-013-1570-9.CrossRefGoogle Scholar
  26. Labropoulou, M., & Eleftheriou, A. (1997). The foraging ecology of two pairs of congeneric demersal fish species: Importance of morphological characteristics in prey selection. Journal of Fish Biology, 50, 324–340.CrossRefGoogle Scholar
  27. Li, Q., Zhang, X., & Yan, C. (2010). Polycyclic aromatic hydrocarbon contamination of recent sediment and marine organisms from Xiamen Bay, China. Archive Environmental Contamination Toxicology, 58, 711–721.CrossRefGoogle Scholar
  28. Livingston, M. E. (1987). Food resource use among five flatfish species (Pleuronectiformes) in Wellington Harbour, New Zealand. New Zealand Journal of Marine and Freshwater Research, 21, 281–293.CrossRefGoogle Scholar
  29. Liu, J., Yan, C., Spencer, K. L., Zhang, R., & Lu, H. (2010). The distribution of acid-volatile sulfide and simultaneously extracted metals in sediments from a mangrove forest and adjacent mudflat in Zhangjiang Estuary, China. Marine Pollution Bulletin, 60, 1209–1216.CrossRefGoogle Scholar
  30. Maruyama, K., Yuan, M., & Otsuki, A. (2000). Seasonal changed in ethylene oxide chain length of poly(oxyethykene)alkylphenyl ether nonionic surfactants in three main rivers in Tokyo. Environmental Science and Technology, 34(2), 343–348.CrossRefGoogle Scholar
  31. Matsuoka, S., Sakakura, R., Takiishi, M., Kurokawa, Y., Kawai, S., & Miyazaki, N. (2005). Determination of natural estrogens in the sediment of coastal area in Japan. Coastal Marine Science, 29, 141–146.Google Scholar
  32. Nakamura, Y. (1998). Nonionic surfactants-history, kind and property and use. Journal of Japan Society of Water Environment, 21, 192–196 (in Japanese).Google Scholar
  33. Nurulnadia, M. Y., Koyama, J., Uno, S., Kokushi, E., Bacolod, E. T., Ito, K., et al. (2013). Bioaccumulation of dietary endocrine disrupting chemicals (EDCs) by polychaete, Perinereis nuntia. Bulletin of Environmental Contamination and Toxicology. doi: 10.1007/s00128-013-1073-9.Google Scholar
  34. Okuda, S. (1937). Spioniform polychaetes from Japan. Journal of the Faculty of Science Hokkaido Imperial University Series 6, Zoology, 5(3), 217–254.Google Scholar
  35. Osaka Prefectural Fisheries Experimental Station (1973–2002). Business report of Osaka Prefectural Fisheries Experimental Station, 1972–2000 (in Japanese).Google Scholar
  36. Petrovic, M., Solé, M., López de Alda, M. J., & Barceló, D. (2002). Endocrine disruptors in sewage treatment plants, receiving river waters, and sediments: Integration of chemical analysis and biological effects on feral carp. Environmental Toxicology & Chemistry, 21, 2146–2156.CrossRefGoogle Scholar
  37. Reddy, S., & Brownawell, B. J. (2005). Analysis of estrogens in sediment from a sewage impacted urban estuary using high performance liquid chromatography/time-of-flight mass spectrometry. Environmental Toxicology and Chemistry, 24(5), 1041–1047.CrossRefGoogle Scholar
  38. Renner, R. (1997). European bans on surfactant trigger transatlantic debate. Environmental Science and Technology, 31, 316A–320A.CrossRefGoogle Scholar
  39. Sakai city. (2001). Local government of Sakai city, Osaka. http://www.city.sakai.osaka.jp/city/info/_koho/houdou.html.
  40. Schlenk, D., Sapozhnikova, Y., Irwin, M. A., Xie, L. T., Hwang, W., Reddy, S., et al. (2005). In vivo bioassay-guided fractionation of marine sediment extracts from the Southern California Bight, USA, for estrogenic activity. Environmental Toxicology and Chemistry, 24, 2820–2826.CrossRefGoogle Scholar
  41. Socha, S. B., & Carpenter, R. (1987). Factors affecting pore water hydrocarbon concentrations in Puget Sound sediments. Geochimica et cosmochimica Acta, 51, 1273–1284.CrossRefGoogle Scholar
  42. Tanghe, T., Devriese, G., & Verstraete, W. (1998). Nonylphenol degradation in lab scale activated sludge units is temperature dependent. Water Research, 32(10), 2889–2896.CrossRefGoogle Scholar
  43. Tanimoto, T., Kawana, K., & Yamaoka, Y. (1984). Grain size parameters and organic matter of bottom sediment in the Seto Island Sea. Rep. Gov. Ind. Res. Inst. Chugoku, Japan, 21, 1–11 (in Japanese with English abstract).Google Scholar
  44. Tanner, P. A., & Leong, L. S. (1997). Microwave vacuum drying of marine sediment: determination of moisture content, metals and total carbon. Analytica Chimica Acta, 342, 247–252.CrossRefGoogle Scholar
  45. Tashiro, Y., Takemura, A., Fujii, H., Takahira, K., & Nakanishi, Y. (2003). Livestock wastes as a source of estrogens and their effects on wildlife of Manko tidal flat, Okinawa. Marine Pollution Bulletin, 47, 143–147.CrossRefGoogle Scholar
  46. Ternes, T. A., Anderson, H., Gilberg, D., & Bonerz, M. (2002). Determination of estrogens in sludge and sediments by liquid extraction and GC/MS/MS. Analytical Chemistry, 74, 3498–3504.CrossRefGoogle Scholar
  47. Thomas, K. V., Balaam, J., Hurst, M., Nedyalkova, Z., & Mekenyan, O. (2004). Potency and characterization of estrogen-receptor agonists in United Kingdom estuarine sediments. Environmental Toxicology and Chemistry, 23, 471–479.CrossRefGoogle Scholar
  48. Tsujimoto, A., Nomura, R., Yasuhara, M., Yamazaki, H., & Yoshikawa, S. (2006). Impact of eutrophication on shallow marine benthic foraminifers over the last 150 years in Osaka Bay, Japan. Marine Micropaleontology, 60, 258–268.CrossRefGoogle Scholar
  49. Vasquez-Duhalt, R., Marquez-Rocha, F., Ponce, E., Licea, A. F., & Viana, M. T. (2005). Nonylphenol, an integrated vision of a pollutant, scientific review. Applied Ecology & Environmental Research, 4(1), 1–25.Google Scholar
  50. Wan, Y., Jin, X., Hu, J., & Jin, F. (2007). Trophic dilution of polycyclic aromatic hydrocarbons (PAHs) in a marine food web from Bohai Bay, North China. Environmental Science & Technology, 41, 3109–3114.CrossRefGoogle Scholar
  51. Wan, Y., Hu, J., Zhang, K., & An, L. (2008). Trophodynamics of polybrominated diphenyl ethers in the marine food web of Bohai Bay, North China. Environmental Science & Technology, 42, 1078–1083.CrossRefGoogle Scholar
  52. White, R., Jobling, S., Hoare, S. A., Sumpter, J. P., & Parker, M. G. (1994). Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology, 135, 175–182.Google Scholar
  53. Wilson, E. O. (1999). The diversity of life (p. 406). London: Penguin.Google Scholar
  54. Woodburn, K. B., Lee, L. S., Rao, P. S. C., & Delfino, J. J. (1989). Comparison of sorption energetics for hydrophobic organic chemicals by synthetic and natural sorbents from methanol/water solvent mixtures. Environmental Science and Technology, 23(4), 407–413.CrossRefGoogle Scholar
  55. Yanagi, T. (1987). Seasonal variations of water temperature and salinity in Osaka Bay. Journal of the Oceanographical Society of Japan, 43, 244–250.CrossRefGoogle Scholar
  56. Yokoyama, H. (1988). Effects of temperature on the feeding activity and growth rate of the spinoid polychaete Paraprionospio sp. (form A). Journal of Experimental Marine Biology and Ecolology, 123, 41–60.CrossRefGoogle Scholar
  57. Yu, Z. Q., Xiao, B. H., Huang, W. L., & Peng, P. (2004). Sorption of steroid estrogens to soils and sediments. Environmental Toxicology and Chemistry, 23, 531–539.CrossRefGoogle Scholar
  58. Zhang, X., Gao, Y., Li, Q., Li, G., Guo, Q., & Yan, C. (2011). Estrogenic compounds and estrogenicity in surface water, sediments, and organisms from Yundang Lagoon in Xiamen, China. Archives of Environmental Contamination and Toxicology, 61, 93–100.CrossRefGoogle Scholar
  59. Zhang, Z., Hibberd, A., & Zhou, J. L. (2008). Analysis of emerging contaminants in sewage effluent and river water: Comparison between spot and passive sampling. Analytica Chimica Acta, 607, 37–44.CrossRefGoogle Scholar
  60. Zhang, X., Li, Q., Li, G., Wang, Z., & Yan, C. (2009). Levels of estrogenic compounds in Xiamen Bay sediment, China. Marine Pollution Bulletin, 58, 1210–1216.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Mohd Yusoff Nurulnadia
    • 1
    • 4
  • Jiro Koyama
    • 2
  • Seiichi Uno
    • 2
  • Asami Kito
    • 3
  • Emiko Kokushi
    • 2
  • Eugene Tan Bacolod
    • 1
  • Kazuki Ito
    • 1
  • Yasutaka Chuman
    • 1
  1. 1.United Graduate School of Agricultural SciencesKagoshima UniversityKagoshimaJapan
  2. 2.Faculty of FisheriesKagoshima UniversityKagoshimaJapan
  3. 3.Graduate School of FisheriesKagoshima UniversityKagoshimaJapan
  4. 4.Faculty of Maritime Studies and Marine SciencesUniversiti Malaysia TerengganuTerengganuMalaysia

Personalised recommendations