Water, Air, & Soil Pollution

, Volume 218, Issue 1–4, pp 19–36 | Cite as

Biomonitoring of Trace Metals (Fe, Cu, and Ni) in the Mangrove Area of Peninsular Malaysia Using Different Soft Tissues of Flat Tree Oyster Isognomon alatus

  • C. K. YapEmail author
  • A. R. Azmizan
  • M. S. Hanif


It is well documented that marine oysters are net bioaccumulators of trace metals and they can be employed as biomonitors of time-integrated measurements of bioavailable metal fractions over their lifetime. In this study, the Malaysian mangrove flat tree oyster Isognomon alatus collected from the estuaries of Lukut River (five sites), Sepang Besar River (one site), and one metal-polluted site at Kg. Pasir Puteh were dissected into muscle, mantle plus gills, byssus, and remaining soft tissues. All the four different soft tissues were analyzed for Fe, Cu, and Ni. Significant spatial differences in the accumulated metal concentrations of the oysters were found between sampling sites, and these could be attributed to anthropogenic inputs including discharges of shrimp ponds (Lukut), animal husbandry (Sepang Besar), sewage, shipping, and industrial effluents (Kg. Pasir Puteh). For Fe, the tissue distribution followed: byssus > mantle plus gill >muscle > remaining soft tissues, while for Cu and Ni, both followed byssus > remaining soft tissues > mantle plus gill > muscle. This indicated that byssus could act as an excretion route for the metals. Based on a correlation analysis between oyster tissues and sediments, selected tissues of I. alatus were shown to be good biomonitors of Ni and Cu contamination, while high regulative capacity of Fe in the oyster tissues could hardly reflect the actual Fe levels in the surroundings. However, the clustering patterns based on metal levels in the four different soft tissues were not in agreement with those based on the geochemical fractions of sediment data. This phenomenon which was due to the metal contamination might not necessarily create high bioavailabilities of metals to the biomonitor I. alatus, which might involve differences in uptake, excretion, and sequestration of metals. Similarly to the Mussel Watch approach, this study points to the very potential use of the different soft tissues of I. alatus as biomonitors for regular biomonitoring in the mangrove area of Peninsular Malaysia.


Biomonitoring Isognomon alatus Trace metals Mangrove area of Peninsular Malaysia 



The authors would like to acknowledge the financial support provided through the Research University Grant Schemes (RUGSs, Vote no. 91986) by Universiti Putra Malaysia.


  1. Acevedo-Figueroa, D., Jimenez, B. D., & Rodríguez-Sierra, C. J. (2006). Trace metals in sediments of two estuarine lagoons from Puerto Rico. Environmental Pollution, 141, 336–342.CrossRefGoogle Scholar
  2. Badri, M. A., & Aston, S. R. (1983). Observation on heavy metal geochemical associations in polluted and non-polluted estuarine sediments. Environmental Pollution, 6(Series B), 181–193.Google Scholar
  3. Boyden, C. R. (1977). Effects of size upon metals content of shellfish. Journal of the Marine Biological Association (United Kingdom), 57, 675–714.CrossRefGoogle Scholar
  4. Brown, B. E., & Kumar, A. J. (1990). Temporal and spatial variations in iron concentrations of tropical bivalves during a dredging event. Marine Pollution Bulletin, 21(3), 118–123.CrossRefGoogle Scholar
  5. Campos, N. H. (1988). Selected bivalves for monitoring of heavy metal contamination in the Colombian Caribbean. In U. Seeliger, L. D. De Lacerda, & S. R. Patchineelam (Eds.), Metals in coastal environments of Latin America (pp. 270–275). Berlin: Springer.Google Scholar
  6. Cunningham, P. A. (1979). The use of bivalve molluscs in heavy metal pollution research. In W. B. Vernberg, A. Calabrese, F. P. Thurberg, & F. J. Vernberg (Eds.), Marine pollution: Functional responses (pp. 183–220). New York: Academic.Google Scholar
  7. Daskalakis, K. K., & O’Connor, T. P. (1995). Normalization and elemental sediment contamination in the coastal United States. Environmental Science & Technology, 29, 47–477.CrossRefGoogle Scholar
  8. Day, R. W., & Quinn, G. P. (1989). Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs, 59, 433–463.CrossRefGoogle Scholar
  9. Eisler, R. (1998). Nickel hazards to fish, wildlife, and invertebrates: A synoptic review. Biological science report USGS/BRD/BSR-1998-0001 contaminant hazard reviews, April 1998 (p. 34). Patuxent Wildlife Research Center, US Geological Survey, Report No. 34.Google Scholar
  10. Ergin, M., Saydam, C., Basturk, O., Erdem, E., & Yoruk, R. (1991). Heavy metal concentrations in surface sediments from the two coastal inlets (Golden Horn Estuary and Izmit Bay) of the northeastern Sea of Marmara. Chemical Geology, 91, 269–285.CrossRefGoogle Scholar
  11. Feng, H., Cochran, J. K., Lwiza, H., Brownawell, B., & Hirschberg, D. J. (1998). Distribution of heavy metal and PCB contaminants in the sediments of an urban estuary: The Hudson River. Marine Environmental Research, 45, 69–88.CrossRefGoogle Scholar
  12. Frias-Espericueta, M. G., Ortiz-Arellano, M. A., Osuna-Lopez, J. I., & Ronson-Paulin, Y. J. A. (1999). Heavy metals in the rock oyster Crassostrea iridescens (Filibranchia: Ostreidae) from Mazatlan, Sinaloa, Mexico. Revista de Biologia Tropical, 47, 843–849.Google Scholar
  13. Hédouin, L., Bustamante, P., Churlaud, C., Pringault, O., Fichez, R., & Warnau, M. (2009). Trends in concentrations of selected metalloid and metals in two bivalves from the coral reefs in the SW lagoon of New Caledonia. Ecotoxicology and Environmental Safety, 72, 372–381.CrossRefGoogle Scholar
  14. Jaffe, R., Leal, I., Alvarado, J., Gardinali, P. R., & Sericano, J. L. (1998). Baseline study on the levels of organic pollutants and heavy metals in bivalves from the Morrocoy National Park, Venezuela. Marine Pollution Bulletin, 36, 925–929.CrossRefGoogle Scholar
  15. Lauenstein, G. G., Robertson, A., & O’Connor, T. P. (1990). Comparison of trace metal data in mussels and oysters from a mussel watch programme of the 1970s with those from a 1980s programme. Marine Pollution Bulletin, 21, 440–447.CrossRefGoogle Scholar
  16. Maanan, M. (2008). Heavy metal concentrations in marine molluscs from the Moroccan coastal region. Environmental Pollution, 153, 176–183.CrossRefGoogle Scholar
  17. Martin, J. M., & Whitfield, M. (1983). The significance of the river input of chemical elements to the ocean. In C. S. Wong, E. Boyle, K. W. Brul, J. D. Burton, & E. D. Goldberg (Eds.), Trace metals in sea water (pp. 265–296). New York: Plenum.Google Scholar
  18. Mostafa, A. R., Al-Alimi, A. K. A., & Barakat, A. O. (2009). Metals in surface sediments and marine bivalves of the Hadhramout coastal area, Gulf of Aden, Yemen. Marine Pollution Bulletin, 58, 308–311.CrossRefGoogle Scholar
  19. Mucha, A. P., Vasconcelos, M. T. S. D., & Bordalo, A. A. (2003). Macrobenthic community in the Doura estuary: Relations with trace metals and natural sediment characteristics. Environmental Pollution, 121, 169–180.CrossRefGoogle Scholar
  20. Nordberg, F. G., Fowler, B. A., Nordberg, M., & Friberg, L. T. (2007). Handbook on the toxicology of metals, 3rd ed. (p. 1024). San Diego: Academic. ISBN 978-0-12-369413-3.Google Scholar
  21. Phelps, H. L., Wright, D. A., & Mihursky, J. A. (1985). Factors affecting trace metal accumulation by estuarine oysters Crassostrea virginica. Marine Ecology Progress Series, 22, 187–197.CrossRefGoogle Scholar
  22. Phillips, D. J. H., & Rainbow, P. S. (1994). Biomonitoring of trace aquatic contaminants (2nd ed.). London: Chapman & Hall.Google Scholar
  23. Presley, B. J., Taylor, R. J., & Boothe, P. N. (1990). Trace metals in Gulf of Mexico oysters. The Science of the Total Environment, 97/98, 551–593.CrossRefGoogle Scholar
  24. Rainbow, P. S. (1995). Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin, 31, 183–192.CrossRefGoogle Scholar
  25. Rainbow, P. S., & Blackmore, G. (2001). Barnacles as biomonitors of trace metal availabilities in Hong Kong coastal waters: Changes in space and time. Marine Environmental Research, 51, 441–463.CrossRefGoogle Scholar
  26. Saed, K., Ismail, A., Omar, H., & Kusnan, M. (2001). Accumulation of heavy metals (Zn, Cu, Pb, Cd) in flat-tree oysters Isognomon alatus exposed to pig farm effluent. Toxicological and Environmental Chemistry, 82, 45–58.CrossRefGoogle Scholar
  27. Saed, K., Ismail, A., Omar, H., & Kusnan, M. (2004). Heavy metal depuration in flat tree oysters Isognomon alatus under field and laboratory conditions. Toxicological and Environmental Chemistry, 86, 171–179.CrossRefGoogle Scholar
  28. Sajwan, K. S., Senthil Kumar, K., Paramasivam, S., Compton, S. S., & Richardson, J. P. (2008). Elemental status in sediment and American oyster collected from Savannah Marsh/Estuarine ecosystem: A preliminary assessment. Archives of Environmental Contamination and Toxicology, 54, 245–258.CrossRefGoogle Scholar
  29. Sbriz, L., Aquino, M. R., Alberto de Rodriguez, N. M., Fowler, S. W., & Sericano, J. L. (1998). Levels of chlorinated hydrocarbons and trace metals in bivalves and nearshore sediments from the Dominican Republic. Marine Pollution Bulletin, 36, 971–979.CrossRefGoogle Scholar
  30. Schi, K. C., & Weisberg, S. B. (1999). Iron as a reference element for determining trace metal enrichment in Southern California coast shelf sediments. Marine Environmental Research, 48, 161–176.CrossRefGoogle Scholar
  31. Silva, C. A. R., Rainbow, P. S., & Smith, B. D. (2003). Biomonitoring of trace metal contamination in mangrove-lined Brazilian coastal systems using the oyster Crassostrea rhizophorea: Comparative study of regions affected by oil, salt pond and shrimp farming activities. Hydrobiologia, 501, 199–206.CrossRefGoogle Scholar
  32. Singh, B. R., & Steinnes, E. (1994). Soil and water contamination by heavy metals. In R. Lal & B. A. Stewart (Eds.), Soil processes and water quality (pp. 233–272). Boca Raton: Lewis.Google Scholar
  33. Yap, C. K. (2010). Normalization of heavy metal concentrations of the tropical coastal surface sediments by using the metal geochemical resistant fraction. Malaysian Applied Biology (in press).Google Scholar
  34. Yap, C. K., Ismail, A., Tan, S. G., & Omar, H. (2002). Concentrations of Cu and Pb in the offshore and intertidal sediments of the west coast of Peninsular Malaysia. Environment International, 28, 467–497.CrossRefGoogle Scholar
  35. Yap, C. K., Ismail, A., & Tan, S. G. (2003a). Background concentrations of Cd, Cu, Pb and Zn in the green-lipped mussel Perna viridis (Linnaeus) from Peninsular Malaysia. Marine Pollution Bulletin, 46, 1043–1048.Google Scholar
  36. Yap, C. K., Ismail, A., & Tan, S. G. (2003b). Effects of total soft tissue and shell thickness on the accumulation of heavy metals (Cd, Cu, Pb and Zn) in the green-lipped mussel Perna viridis (Linnaeus). Russian Journal of Marine Biology, 29(5), 323–327.CrossRefGoogle Scholar
  37. Yap, C. K., Ismail, A., & Tan, S. G. (2003c). Cd and Zn in the straits of Malacca and intertidal sediments of the west coast of Peninsular Malaysia. Marine Pollution Bulletin, 46, 1348–1353.Google Scholar
  38. Yap, C. K., Ismail, A., Tan, S. G., & Rahim Ismail, A. (2004). The impact of anthropogenic activities on heavy metal (Cd, Cu, Pb and Zn) pollution: Comparison of the metal levels in green-lipped mussel Perna viridis (Linnaeus) and in the sediment from a high activity site at Kg. Pasir Puteh and a relatively low activity site at Pasir Panjang. Pertanika Journal of Tropical Agricultural Science, 27(1), 73–78.Google Scholar
  39. Yap, C. K., Ismail, A., & Tan, S. G. (2005). Byssus of the green-lipped mussel Perna viridis (Linnaeus) as a biomonitoring material for Zn. Russian Journal of Marine Biology, 31(2), 102–108.CrossRefGoogle Scholar
  40. Yap, C. K., Ismail, A., Edward, F. B., Tan, S. G., & Siraj, S. S. (2006). Use of different soft tissues of Perna viridis as biomonitors of bioavailability and contamination by heavy metals (Cd, Cu, Fe, Pb, Ni and Zn) in a semi-enclosed intertidal water, the Johore Straits. Toxicological and Environmental Chemistry, 88(4), 683–695.CrossRefGoogle Scholar
  41. Yap, C. K., Ismail, A., Ismail, A. R., & Tan, S. G. (2006). Biomonitoring of ambient concentrations of cadmium, copper, lead and zinc in the coastal wetland water by using gills of the green-lipped mussel Perna viridis. Wetland Science, 4(4), 247–252.Google Scholar
  42. Zar, J. H. (1996). Biostatistical analysis (3rd ed.). New Jersey: Prentice-Hall.Google Scholar
  43. Zhang, J., & Liu, C. L. (2002). Riverine composition and estuarine geochemistry of particulate metals in China—Weathering features, anthropogenic impact and chemical fluxes. Estuarine, Coastal and Shelf Science, 54, 1051–1070.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  1. 1.Department of Biology, Faculty of ScienceUniversiti Putra MalaysiaSerdangMalaysia

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