Skip to main content
SpringerLink
Log in

Digestive Cecum and Tissue Redistribution in Gills of Telescopium telescopium as Indicators of Ni Bioavailabilities and Contamination in Tropical Intertidal Areas

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

The relationships between the Ni concentrations of the mudflat snails Telescopium telescopium and the surface sediments have not been reported yet from tropical intertidal areas. In this study, telescope snails and surface sediments were collected from 18 geographical sampling sites in intertidal areas of Peninsular Malaysia. The concentrations of Ni were measured in seven different soft tissues of the snails namely foot, cephalic tentacles, mantle, muscle, gill, digestive cecum, and remaining soft tissues. It was found that different concentrations of Ni were found in the different soft tissues, indicating different mechanisms of sequestration and regulation of Ni in these different tissues. By comparing the Ni concentrations in the similar tissues, spatial variations of Ni were found in the different sampling sites although there was no consistent pattern of Ni in these sites. The highest Ni variation based on the ratio of maximum to minimum values indicated that cephalic tentacle and foot were the main organs having high Ni variation. The use of correlation analysis and multiple linear stepwise regression analysis revealed that digestive cecum of T. telescopium could be used to reflect the Ni contamination of the sampling site. Also, the digestive cecum and gill were found to be the main bioaccumulation and storage sites for Ni. From the Ni accumulation patterns in all the populations investigated, tissue redistributions of Ni in gill was identified and could be proposed as an indicator of high Ni bioavailability and contamination in the sampling site. To our knowledge, this is the first and most comprehensive study on Ni accumulation in the different soft tissues of T. telescopium from tropical intertidal areas, in relation to the sediment data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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.

    CAS  Google Scholar 

  • Balogh, K. V., Fernandez, D. S., & Salanki, J. (1988). Heavy metal concentrations of Lymnaea stagnalis L. in the environs of Lake Balaton (Hungary). Water Research, 22(10), 1205–1210.

    Article  Google Scholar 

  • Bintal, A., Ismail, A., Arshad, A., Yap, C. K., & Kamarudin, M. S. (2009). Anthropogenic impacts on heavy metal concentrations in the coastal sediments of Dumai, Indonesia. Environmental Monitoring and Assessment, 148, 291–305.

    Article  Google Scholar 

  • Chapman, P. M., Allarfd, P. J., & Vigers, G. A. (1999). Development of sediment quality values for Hong Kong special administrative region: A possible model for other jurisdictions. Marine Pollution Bulletin, 38, 161–169.

    Article  CAS  Google Scholar 

  • Cuong, D. T., & Obbard, N. (2006). Metal speciation in coastal marine sediments from Singapore using a modified BCR sequential extraction procedure. Applied Geochemistry, 21, 1335–1346.

    Article  CAS  Google Scholar 

  • Daka, E. R. (2005). Heavy metal concentrations in Littorina saxatilis and Enteromorpha intestinalis from Manx Estuaries. Marine Pollution Bulletin, 46(6), 784–791.

    Article  Google Scholar 

  • Daka, E. R., & Hawkins, S. J. (2006). Interactive effects of copper, cadmium and lead on zinc accumulation in the gastropod molluscs Littorina saxatilis. Water, Air, & Soil Pollution, 171, 19–28.

    Article  CAS  Google Scholar 

  • Dang, T. C., Stephane, B., Oliver, W., Subramaniam, K., Kae, S. W., Sivasothi, N., et al. (2005). Heavy metal contamination in mangrove habitats of Singapore. Marine Pollution Bulletin, 50, 1713–1744.

    Article  Google Scholar 

  • 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. Patuxent Wildlife Research Center, U.S. Geological Survey. Report No. 34. pp 95

  • Gundacker, C. (2000). Comparison of heavy metal bioaccumulation in freshwater molluscs of urban river habitats in Vienna. Environmental Pollution, 110, 61–71.

    Article  CAS  Google Scholar 

  • Hamed, M. A., & Emara, A. M. (2006). Marine molluscs as biomonitors for heavy metal levels in the Gulf of Suez, Red Sea. Journal of Marine Systems, 60, 220–234.

    Article  Google Scholar 

  • Ismail, A., & Safahieh, A. (2004). Copper and Zinc in intertidal surface sediment and Telescopium telescopium from Lukut River, Malaysia. Coastal Marine Science, 29(2), 111–115.

    Google Scholar 

  • Jones, G. B., Mercurio, P., & Olivier, F. (2000). Zinc in fish, crabs, oysters and mangrove flora and fauna from Cleveland Bay. Marine Pollution Bulletin, 41, 345–352.

    Article  CAS  Google Scholar 

  • Khalid, R. A., Patrick, W. H., & Gambrel, P. (1978). Effect of dissolved oxygen on chemical transformations of heavy metals, phosphorus, and nitrogen in an estuarine sediment. Estuarine and Coastal Marine Science, 6(1), 21–35.

    Article  CAS  Google Scholar 

  • Lefcort, H. D., Abbott, P., Cleary, D. A., Howell, E., Keller, N. C., & Smith, M. M. (2004). Aquatic snails from mining sites have evolved to detect and avoid heavy metals. Archives of Environmental Contamination and Toxicology, 46, 478–484.

    Article  CAS  Google Scholar 

  • Li, Q. S., Wu, Z. F., Chu, B., Zhang, N., Czi, S. S., & Fang, J. H. (2007). Heavy metals in the coastal wetland sediments of the Pearl River Estuary, China. Environmental Pollution, 149, 158–164.

    Article  CAS  Google Scholar 

  • Liang, L. N., He, B., Jiang, G. B., Chen, D. Y., & Yao, Z. W. (2004). Evaluation of mollusks as biomonitors to investigate heavy metal contaminations along the Chinese Bohai Sea. Science of the Total Environment, 324, 105–113.

    Article  CAS  Google Scholar 

  • Lim, P. E., & Kiu, M. Y. (1995). Determination and speciation of heavy metals in sediments of the Juru River, Penang, Malaysia. Environmental Monitoring and Assessment, 35, 85–95.

    Article  CAS  Google Scholar 

  • Lobel, P. B., Mogie, P., Wright, D. A., & Wu, B. L. (1982). Metal accumulation in four molluscs. Marine Pollution Bulletin, 13(5), 170–174.

    Article  CAS  Google Scholar 

  • Long, E. R., Macdonald, D. D., Smith, S. L., & Calder, F. D. (1995). Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environmental Management, 19, 81–97.

    Article  Google Scholar 

  • Luoma, S. N., & Rainbow, P. S. (2005). Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environmental Science & Technology, 39(7), 1921–1931.

    Article  CAS  Google Scholar 

  • Malaysian DOE. (2008). Department of Environment Malaysia. Malaysia Environmental Quality Report 2007. Department of Environment, Ministry of Natural Resources and Environment, Malaysia. Sasyaz Kreatif Sdn. Bhd., Petaling Jaya. pp.82

  • Manly, R., & George, W. O. (1977). The occurrence of some heavy metals in populations of the freshwater mussel Anodonta anatina (L.) from the River Thames. Environmental Pollution, 14, 139–154.

    Article  CAS  Google Scholar 

  • Nair, N. N., & Saraswathy, M. (1971). The biology of wood-boring teredinid molluscs. Marine Biology, 9, 335–509.

    Article  Google Scholar 

  • Negri, A., Burns, K., Boyle, L., Brinkman, D., & Webster, N. (2006). Contamination in sediments, bivalves and sponges of McMurdo Sound, Antarctica. Environmental Pollution, 143, 456–467.

    Article  CAS  Google Scholar 

  • Nott, J. A., & Nicolaidou, A. (1989). Metals in gastropods—metabolism and bioreduction. Marine Environmental Research, 28(1–4), 201–205.

    Article  CAS  Google Scholar 

  • Peerzada, N., Eastbrook, C., & Guinea, M. (1990). Heavy metal concentration in Telescopium from Darwin Harbour, N.T. Australia. Marine Pollution Bulletin, 21(6), 307–308.

    Article  CAS  Google Scholar 

  • Phillips, D. H., & Rainbow, P. S. (1993). Biomonitoring of trace aquatic contaminants. London: Elsevier Applied Science.

    Book  Google Scholar 

  • Pynnonen, K. (1991). Accumulation of 45Ca in the freshwater unionids Anodonta anatina and Unio tumidus, as influenced by water hardness, protons, and aluminium. The Journal of Experimental Zoology, 260, 18–27.

    Article  CAS  Google Scholar 

  • Rainbow, P. S. (1995). Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin, 31(4–12), 183–192.

    Article  CAS  Google Scholar 

  • Rainbow, P. S. (1997). Trace metal accumulation in marine invertebrates: marine biology or marine chemistry? Journal of the Marine Biological Association of the UK, 77, 195–210.

    Article  CAS  Google Scholar 

  • Rainbow, P. S., & Phillips, D. J. H. (1993). Cosmopolitan biomonitors of trace metals. Marine Pollution Bulletin, 26(11), 595–601.

    Article  Google Scholar 

  • Sadiq, M. (1992). Toxic metal chemistry in marine environments. New York: Marcel Dekker. 390p.

    Google Scholar 

  • Salomons, W., & Förstner, U. (1984). Metals in hydrocycle (p. 349p). Berlin: Springer.

    Book  Google Scholar 

  • Szefer, P., Frelek, K., Szefer, K., Lee, C. B., Kim, B. S., Warzocha, J., et al. (2002). Distribution and relationships of trace metals in soft tissue, byssus and shells of Mytilus edulis trossulus from the southern Baltic. Environmental Pollution, 120, 423–444.

    Article  CAS  Google Scholar 

  • Takarina, N. D., Browne, D. R., & Risk, M. J. (2004). Speciation of heavy metals in coastal sediments of Semarang Indonesia. Marine Pollution Bulletin, 49, 854–874.

    Article  Google Scholar 

  • Talbot, V., & Magee, R. J. (1978). Naturally-occuring heavy metal binding proteins in invertebrates. Archives of Environmental Contamination and Toxicology, 7, 73–81.

    Article  CAS  Google Scholar 

  • Tam, N. F. Y., & Wong, Y. S. (2000). Spatial variation of heavy metals in surface sediments of Hong Kong Mangrove swamps. Environmental Pollution, 110, 195–205.

    Article  CAS  Google Scholar 

  • Taylor, A., & Maher, W. (2006). The use of two marine gastropods, Austrocochlea constricta and Bembicium auratum, as biomonitors of zinc, cadmium, and copper exposure: Effect of tissue distribution, gender, reproductive state, and temporal variation. Journal of Coastal Research, 22(2), 298–306.

    Article  Google Scholar 

  • Usero, J., Morillo, J., & Gracia, I. (2005). Heavy metal concentrations in molluscs from the Atlantic coast of southern Spain. Chemosphere, 59(8), 1175–1181.

    Article  CAS  Google Scholar 

  • USPHS (U. S. Public Health Service) (1993) Toxicological profile for nickel. U.S. Public Health Service, Agency for Toxic Substances and Disease Registry, Atlanta, Georgia. Report TP-92/14. 158 pp

  • Viarengo, A., Palmero, S., Zanicchi, G., Capelli, R., Vaissiere, R., & Orunesu, M. (1985). Role of metallothioneins in Cu and Cd accumulation and elimination in the gill and digestive gland cells of Mytilus galloprovincialis Lam. Marine Environmental Research, 16, 23–36.

    Article  CAS  Google Scholar 

  • WHO (World Health Organization). (1991). Nickel. Environmental Health Criteria 108 (p. 383). Geneva: WHO.

    Google Scholar 

  • Wood, A. K., Ahmad, Z., Shazili, N. A., Yaakob, R., & Carpenter, R. (1997). Geochemistry of sediments in Johore Strait between Malaysia and Singapore. Continental Shelf Research, 10, 1207–1228.

    Article  Google Scholar 

  • 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, 467–479.

    Article  CAS  Google Scholar 

  • Yap, C. K., Tan, S. G., Ismail, A., & Omar, H. (2002). Genetic variation of green-lipped mussel Perna viridis (Linnaeus) from the west coast of Peninsular Malaysia. Zoological Studies, 41(4), 376–387.

    CAS  Google Scholar 

  • Yap, C. K., Ismail, A., & Tan, S. G. (2003). Cd and Zn in the straits of Malacca and intertidal sediments of the west coast of Peninsular Malaysia. Marine Pollution Bulletin, 46, 1348–1353.

    CAS  Google Scholar 

  • Yap, C. K., Ismail, A., Tan, S. G., & Ismail, R. (2004). Assessment of different soft tissues of the green-lipped mussel Perna viridis (Linnaeus) as biomonitoring agents of Pb: Field and laboratory studies. Water, Air, & Soil Pollution, 153, 253–268.

    Article  CAS  Google Scholar 

  • Yap, C. K., Ismail, A., Cheng, W. H., Edward, F. B., & Tan, S. G. (2006a). Crystalline style and byssus of Perna viridis as indicators of Ni bioavailabilities and contamination in coastal waters of Peninsular Malaysia. Malaysian Applied Biology, 35(1), 7–13.

    Google Scholar 

  • Yap, C. K., Ismail, A., Cheng, W. H., & Tan, S. G. (2006b). Crystalline style and tissue redistribution in Perna viridis as indicators of Cu and Pb bioavailabilities and contamination in coastal waters. Ecotoxicology and Environmental Safety, 63, 413–423.

    Article  CAS  Google Scholar 

  • Yap, C. K., Ismail, A., Edward, F. B., Tan, S. G., & Siraj, S. S. (2006c). 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(1–4), 683–695.

    Article  CAS  Google Scholar 

  • Yap, C. K., Ismail, A., Rahim Ismail, A., & Tan, S. G. (2006d). Biomonitoring of ambient concentrations of Cd, Cu, Pb and Zn in the coastal wetland water by using gills of the green-lipped mussel Perna viridis. Wetland Science, 4(4), 247–252.

    Google Scholar 

  • Yap, C. K., Choh, M. S., Franklin, E. B., Ismail, A., & Tan, S. G. (2006e). Comparison of heavy metal concentration in surface sediment of Tanjung Piai Wetland with other sites receiving anthropogenic inputs along the southwestern coast of Peninsular Malaysia. Wetland Science, 4, 48–57.

    Google Scholar 

  • Yap, C. K., Ismail, A., Pang, B. H., Yeow, K. L., Tan, S. G., & Siraj, S. S. (2006f). Elevated heavy metal concentrations in surface sediments collected from the drainages of the Sri Serdang Industrial Area, Malaysia. Malaysian Applied Biology, 35(2), 35–40.

    Google Scholar 

  • Yap, C. K., Pang, B. H., Fairuz, M. S., Hoo, Y. I., & Tan, S. G. (2007). Heavy metal (Cd, Cu, Ni, Pb, and Zn) pollution in surface sediments collected from drainages receiving different anthropogenic sources from Peninsular Malaysia. Wetland Science, 5(2), 97–104.

    Google Scholar 

  • Yap, C. K., Fairuz, M. S., Cheng, W. H., & Tan, S. G. (2008). Distribution of Ni and Zn in the surface sediments collected from drainages and intertidal area in Selangor. Pertanika Journal of Tropical Agricultural Science, 31(1), 79–90.

    Google Scholar 

  • Yap, C. K., & Noorhaidah, A. (2008). An evidence of Pb redistribution in the different soft tissues of Telescopium telescopium collected from a Pb-contaminated intertidal site. Asian Journal of Microbiology, Biotechnology and Environmental Sciences, 10(3), 463–468.

    Google Scholar 

  • Yap, C. K., Fairuz, M. S., Nelson, C., Noorhaidah, A., & Tan, S. G. (2008). Comparison of heavy metal concentrations in the different parts of Telescopium telescopium collected from a relatively less polluted site at Sungai Janggut and a polluted site at Kuala Juru. Malaysian Fisheries Journal, 7(1), 41–46.

    Google Scholar 

  • Yap, C. K., Noorhaidah, A., Azlan, A., Ismail, A., Siraj, S. S., & Tan, S. G. (2009). Telescopium telescopium as potential biomonitors of Cu, Zn, and Pb for the tropical intertidal area. Ecotoxicology and Environmental Safety, 72, 496–506.

    Article  CAS  Google Scholar 

  • Yap, C. K., Edward, F. B., & Tan, S. G. (2010). Heavy metal concentrations (Cu, Pb, Ni and Zn) in the surface sediments from a semi-enclosed intertidal water, the Johore Straits: Monitoring data for future reference. Journal of Sustainable Science and Management, 5(2), 44–57.

    CAS  Google Scholar 

  • Yap, C. K. (2010). High metal contamination and bioavailability might not be necessarily related to high human activity by direct observation: Evidence from metal data in sediments and intertidal snails collected from an unknown anthropogenic site in Malaysia. Asian Journal of Microbiology, Biotechnology and Environmental Sciences, 2(1), 1–5.

    Google Scholar 

  • Yap, C. K., & Pang, B. H. (2011). Anthropogenic concentrations of Cd, Ni and Zn in the intertidal and drainage sediments collected from north western Peninsular Malaysia. Pertanika Journal of Science & Technology, 19(1), 93–107.

    Google Scholar 

  • Yap, C. K., & Wong, C. H. (2011). Assessment Cu, Ni and Zn pollution in the surface sediments in the southern Peninsular Malaysia using cluster analysis, ratios of geochemical nonresistant to resistant fractions, and geochemical indices. Environment Asia, 4(1), 53–61.

    Google Scholar 

  • Yüzereroğlu, T. A., Gök, G., Coğun, H. Y., Firat, O., Aslanyavrusu, S., Maruldali, O., et al. (2010). Heavy metals in Patella caerulea (Mollusca, Gastropoda) in polluted and non-polluted areas from the Iskenderun Gulf (Mediterranean Turkey). Environmental Monitoring and Assessment, 176(1–4), 257–264.

    Article  Google Scholar 

  • Zhang, L., Ye, X., Feng, H., Jing, Y., Ouyang, T., Yu, X., et al. (2007). Heavy metal contamination in western Xiamen Bay sediments and its vicinity, China. Marine Pollution Bulletin, 54, 974–982.

    Article  CAS  Google Scholar 

  • Zhang, W., Feng, H., Chang, J., Qu, J., Xie, H., & Yu, X. (2009). Heavy metal contamination in surface sediments of Yangtze River intertidal zone: An assessment from different indexes. Environmental Pollution, 157, 1533–1543.

    Article  CAS  Google Scholar 

  • Zar, J. H. (1996). Biostatistical analysis (3rd ed.). New Jersey: Prentice Hall. 662 p.

    Google Scholar 

Download references

Acknowledgements

The authors wish to acknowledge the financial support provided through the Fundamental Research Grant Scheme, [Vote no.: 552403], by the Malaysian Ministry of Higher Education.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

    C. K. Yap & A. Noorhaidah

  2. Department of Cell and Molecular Biology, Faculty of Biotechnology and Bimolecular Sciences, Universiti Putra Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

    S. G. Tan

Authors
  1. C. K. Yap
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Noorhaidah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. G. Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. K. Yap.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yap, C.K., Noorhaidah, A. & Tan, S.G. Digestive Cecum and Tissue Redistribution in Gills of Telescopium telescopium as Indicators of Ni Bioavailabilities and Contamination in Tropical Intertidal Areas. Water Air Soil Pollut 223, 2891–2905 (2012). https://doi.org/10.1007/s11270-012-1073-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-012-1073-0

Keywords

Search

Navigation