Environmental Monitoring and Assessment

, Volume 186, Issue 4, pp 2465–2485 | Cite as

Assessment of trace elements in the shell layers and soft tissues of the pearl oyster Pinctada radiata using multivariate analyses: a potential proxy for temporal and spatial variations of trace elements

  • N. Pourang
  • C. A. Richardson
  • S. R. N. Chenery
  • H. Nasrollahzedeh


Concentrations of trace elements (Cd, Cu, Ni, Pb, V, and Zn) were determined in the soft tissues (adductor muscle and gills) of the pearl oyster Pinctada radiata and surficial sediments from two sampling sites located in the northern part of the Persian Gulf by Graphite Furnace Atomic Absorption Spectrophotometer (GFAAS). Moreover, the levels of Li, Mg, Al, Mn, Fe, Cu, Sr, Ba, Pb, and Zn were measured in two shell layers (prismatic and nacreous) using Laser Ablation Inductively Coupled Plasma Mass Spectrometer (LA-ICP-MS). There were significant differences between the sampling sites with regard to mean concentrations of Cu, Mn, and Al in the prismatic layers of the shells. But in terms of the soft tissues, only in the case of Ni accumulation in the muscle significant differences between the sites could be observed. No significant differences could be found between the sites from the elements concentrations in the sediments point of view. The levels of Cd, Cu, Ni, and Zn in the gills were markedly higher than those in the muscle. Concentrations of Mn, Mg, Li, and Cu in the prismatic layer were significantly higher than in the nacreous but the reverse case could be found for Sr. The patterns of metal occurrence in the selected tissues, shell layers, and sediments exhibited the following descending order: Zn, Ni > Cd, Cu > V, and Pb and Zn, Ni, Cd > Cu, V, and Pb for muscle and gills, respectively; Zn > Cu, Ni, Pb, Cd, and V for sediments; Mg > Sr, Mn, Li, Al, Fe, Ba, Cu, Pb, and Zn for the prismatic layer; and Sr, Mg > Mn, Al, Fe, Li, Ba, Cu, Pb, and Zn for the nacreous layer. In most cases, the temporal variations of the elements levels in the prismatic layer were clearer than those in the nacreous layer (especially for Li, Mg, Mn, Pb, and Fe). Comparison of the gained data from this study with the other relevant researches shows that in most cases the levels of the elements in this investigation either fell within the range for other world areas or were lower. Generally, it can be concluded that the shell (especially prismatic layer) of P. radiata can be considered as a suitable proxy for temporal and spatial variations of the trace elements (and probably some environmental parameters) in the study area.


Trace elements Environmental proxy Pinctada radiata Shell layers Soft tissues Sediments 



A large part of this project was funded by Iran Fisheries Research Institute. The authors express their gratitude to the personnel of the Persian Gulf and Oman Sea Ecological Research Center especially M.S. Mortazavi, N. Aghajeri, E. Kamali for their assistance in the sampling, sample preparation and analysis of the sediments and soft tissues.


  1. Abdullah, M. H., Sidi, J., & Aris, A. Z. (2007). Heavy Metals (Cd, Cu, Cr, Pb and Zn) in Meretrix meretrix Roding, Water and Sediments from Estuaries in Sabah, North Borneo. International Journal of Environmental & Science Education, 2(3), 69–74.Google Scholar
  2. Al-Arfaj, A., & Alam, I. A. (1993). Chemical characterization of sediments from the Gulf area after the 1991 oil spill. Marine Pollution Bulletin, 27, 97–101.CrossRefGoogle Scholar
  3. Al-Ghadban, A. N., Abdali, F., & Massoud, M. S. (1998). Sedimentation rate and bioturbation in the Arabian Gulf. Environment International, 24, 23–31.CrossRefGoogle Scholar
  4. Al-Husaini., I.S.I., (2010). Heavy metals in marine sediments, water and fish of single buoy moorings (SBM3), Mina Al Fahal, Sultanate of Oman. Masters thesis, Universiti Teknologi Malaysia, Faculty of Science. 97 pp.Google Scholar
  5. Al-Madfa, H., Abdel-Moati, M. A. R., & Al-Gimaly, F. H. (1998). Pinctada radiata (Pearl Oyster): A Bioindicator for Metal Pollution Monitoring in the Qatari Waters (Persian Gulf). Bulletin of Environmental Contamination and Toxicology, 60, 245–251.CrossRefGoogle Scholar
  6. Al-Sayed, H. A., Mahasneh, A. M., & Al-Saad, J. (1994). Variations of trace metal concentrations in seawater and pearl oyster Pinctada radiata from Bahrain (Persian Gulf). Marine Pollution Bulletin, 28, 370–374.CrossRefGoogle Scholar
  7. Alyahya, H., El-Gendy, A. H., Al-Farraj, S., & El-Hedeny, M. (2011). Evaluation of heavy metal pollution in the Arabian Gulf using the clam Meretrix meretrix Linnaeus, 1758. Water, Air, and Soil Pollution, 214, 499–507.CrossRefGoogle Scholar
  8. ANZECC/ARCMANZ, (2000). Australian and New Zealand Guidelines for Fresh and Marine Water Quality: Volume 2 - Aquatic Ecosystems - Rationale and Background Information. Australian and New Zealand Environment and Conservation Council, Agriculture and Resource Management Council of Australia and New Zealand
  9. Bairwise, A. J. G. (1990). Role of nickel and vanadium in petroleum classification. Energy & Fuels, 4, 647–652.CrossRefGoogle Scholar
  10. Beone, G. M., Cattani, I., Fontanella, M. C., & Ravera, O. (2011). Relationship between element concentrations and body size in the Lake Maggiore population of Unio pictorum mancus (Mollusca, Bivalvia). Journal of Limnology, 70(2), 283–292.CrossRefGoogle Scholar
  11. Biksham, G., Subramanian, V., & Griken, R. (1991). Heavy metal distribution in the Godavari river basin. Environmental Geology and Water Sciences, 17, 117–126.CrossRefGoogle Scholar
  12. Bonneris, E., Giguere, A., Perceval, O., Buronfosse, T., Masson, S., Hare, L., & Campbell, P. G. C. (2005). Sub-cellular partitioning of metals (Cd, Cu, Zn) in the gills of a freshwater bivalve, Pyganodon grandis: role of calcium concretions in metal sequestration. Aquatic Toxicology, 71, 319–334.CrossRefGoogle Scholar
  13. Bou-Olayan, A. H., Al-Mattar, S., Al-Yakoob, S. A., & Al-Hazeem, S. (1995). Accumulation of Lead, Cadmium, Copper and Nickel by Pearl Oyster, Pinctada radiata, from Kuwait Marine Environment. Marine Pollution Bulletin, 30, 211–214.CrossRefGoogle Scholar
  14. Bowen, H. J. M. (1979). Environmental chemistry of the elements. London: Academic Press. 333 pp.Google Scholar
  15. Boxall, A. B. A., Comber, C. D., Conrad, A. U., Howcroft, J., & Zaman, N. (2000). Inputs, monitoring and fate modeling of antifouling biocides in UK estuaries. Marine Pollution Bulletin, 40, 898–905.CrossRefGoogle Scholar
  16. Buchman, M.F., (1999). NOAA Screening Quick Reference Table, NOAA HAZMAT Report 99–1, Seattle, WA, Coastal Protection and Restoration Division, National Oceanic and Atmospheric Administration. 12 pp.Google Scholar
  17. Campbell, P. G. C., & Tessier, A. (1996). Ecotoxicology of metals in the aquatic environment Geochemical aspects. In M. C. Newman & C. H. Jagoe (Eds.), Ecotoxicology: A hierarchical treatment (pp. 11–58). Boca Raton: Lewis Publishers.Google Scholar
  18. Carroll, M., & Romanek, C. S. (2008). Shell layer variation in trace element concentration for the freshwater bivalve Elliptio complanata. Geo-Marine Letters, 28, 369–381.CrossRefGoogle Scholar
  19. Carvalho, J. C., Anfossi, D., Trini Castelli, S., & Degrazia, G. A. (2002). Application of a model system for the study of transport and diffusion in complex terrain to the tract experiment. Atmospheric Environment, 36, 1147–1161.CrossRefGoogle Scholar
  20. CCME, (1999). Canadian sediment quality guidelines for the protection of aquatic life: Summary tables. In: Canadian environmental quality guidelines, Canadian Council of Ministers for the Environment (CCME), Winnipeg.Google Scholar
  21. Cempel, M., & Nikel, G. (2006). Nickel: A Review of Its Sources and Environmental Toxicology. Polish Journal of Environmental Studies, 15(3), 375–382.Google Scholar
  22. Chang, F., Li, G. C., Haws, M., & Niu, T. H. (2007). Element concentrations in shell of Pinctada margaritifera from French Polynesia and evaluation for using as a food supplement. Food Chemistry, 104, 1171–1176.CrossRefGoogle Scholar
  23. Clark, R.B., (2001). Marine Pollution. 5th Edition, Oxford University Press, 237 pp.Google Scholar
  24. De Mora, S., Fowler, S. W., Wyse, E., & Azemard, S. (2004). Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf and Gulf of Oman. Marine Pollution Bulletin, 49, 410–424.CrossRefGoogle Scholar
  25. DFWA, (2002). Application to Environment Australia on the Pearl Oyster Fishery. Department of Fisheries Western Australia (DFWA), 94 pp.Google Scholar
  26. Dunca, E., Mutvei, H., Göransson, P., Mörth, C. M., Schöne, B. R., Whitehouse, M. J., Elfman, M., & Baden, S. P. (2009). Using ocean quahog (Arctica islandica) shells to reconstruct palaeoenvironment in Öresund, Kattegat and Skagerrak, Sweden. International Journal of Earth Sciences, 98, 3–17.CrossRefGoogle Scholar
  27. Eisler, R., (1998). Nickel hazards to fish, wildlife, and invertebrates: A synoptic review. U.S Geological Survey. Biological Scientific Report 34. 95 pp.Google Scholar
  28. Ejlali Khanghah, K., Abdolalian, A., & Rameshi, H. (2007). Population dynamics of pearl oyster Pinctada radiata west of Lavan Island of the Persian Gulf, Iran. Iranian Scientific Fisheries journal, 3, 1–10.Google Scholar
  29. Emara, A.M., (1999). Surveillance and biological studies of the intertidal molluscs along the western coast of the Gulf of Suez, Egypt. Ph.D. Thesis, Tanta University, Faculty of Science, Zoology Department, 218 pp.Google Scholar
  30. ETWB, (2002). Management of dredged/excavated sediment. Environment, Transport and Works Bureau, Technical Circular (Works) No. 34. Hong Kong, 17 pp.Google Scholar
  31. FAO, (1991). Pearl oyster farming and pearl culture. FAO/UNDP Regional Seafarming Project. 103 pp.Google Scholar
  32. Farahani, M.R.H., (1998). Investigation of oil Pollution in Lavan Island shore line water. the 8th Conference of oil , Gas & Petrochemical Industries, Tehran , Iran. 18–24.Google Scholar
  33. Foster, L. C., Finch, A. A., Allison, N., Andersson, C., & Clarke, L. J. (2008). Mg in aragonitic bivalve shells: Seasonal variations and mode of incorporation in Arctica islandica. Chemical Geology, 254, 113–119.CrossRefGoogle Scholar
  34. Fowler, S. W., Readman, J. W., Oregioni, B., Villeneuve, J. P., & McKay, K. (1993). Petroleum hydrocarbons and trace metals in nearshore Gulf sediments and biota before and after the 1991 war: an assessment of temporal and spatial trends. Marine Pollution Bulletin, 27, 171–182.CrossRefGoogle Scholar
  35. Franco, J., Borja, Á., Solaun, O., & Pérez, V. (2002). Heavy metals in molluscs from the Basque Coast (Northern Spain): results from an 11-year monitoring programme. Marine Pollution Bulletin, 44(9), 973–976.CrossRefGoogle Scholar
  36. Freitas, P. S., Clarke, L. J., Kennedy, H., Richardson, C. A., & Abrantes, F. (2006). Environmental and biological controls on elemental (Mg/Ca, Sr/Ca and Mn/Ca) ratios in shells of the king scallop Pecten maximus. Geochimica et Cosmochimica Acta, 70, 5119–5133.CrossRefGoogle Scholar
  37. Gagnon, C., Gagné, F., Turcotte, P., Saulnier, I., Blaise, C., Salazar, M. H., & Salazar, S. M. (2006). Exposure of caged mussels to metals in a primary-treated municipal wastewater plume. Chemosphere, 62(6), 998–1010.CrossRefGoogle Scholar
  38. Ganor, E., Altshuller, S., Foner, H. A., Brenner, S., & Gabay, J. (1988). Vanadium and nickel in dustfall as indicators of power plant pollution. Water, Air, and Soil Pollution, 42, 241–252.Google Scholar
  39. Gargouri, D., Azri, C., Serbaji, M. M., Jedoui, Y., & Montacer, M. (2011). Heavy metal concentrations in the surface marine sediments of Sfax Coast, Tunisia. Environmental Monitoring and Assessment, 175(1–4), 519–530.CrossRefGoogle Scholar
  40. Gillikin, D., Dehairs, F., Baeyens, W., Navez, J., Lorrain, A., & André, L. (2005). Inter- and intra-annual variations of Pb/Ca ratios in clam shells (Mercenaria mercenaria): A record of anthropogenic lead pollution? Marine Pollution Bulletin, 50(12), 1530–1540.CrossRefGoogle Scholar
  41. Gnanadesikan, R., (1997). Methods for statistical data analysis of multivariate observations. 2nd ed., John Wiley & Sons, 384 pp.Google Scholar
  42. Goksu, M. Z. L., Akar, M., Çevik, F., & Fındık, Ö. (2005). Bioaccumulation of Some Heavy Metals (Cd, Fe, Zn, Cu) in Two Bivalvia Species (Pinctada radiata Leach, 1814 and Brachidontes pharaonis Fischer, 1870). The Turkish Journal of Veterinary and Animal Sciences, 29, 89–93.Google Scholar
  43. Grimwood, M.J.,Dixon, E., (1997). Assessment of risks posed by list II metals of sensitive marine areas (SMAs) and adequacy of existing environmental quality standards (EQSs) for SMA protection. Report to English Nature, 32 pp.Google Scholar
  44. Gundacker, C. (2000). Comparison of heavy metal bioaccumulation in freshwater mollusks of urban river habitats in Vienna. Environmental Pollution, 110, 61–71.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. Haque, A. M., Szymelfenig, M., & Węsławski, M. (1997). Spatial and seasonal changes in the sandy littoral zoobenthos of the Gulf of Gdańsk. Oceanologia, 39, 299–324.Google Scholar
  47. Hédouin, L., Metian, M., Teyssié, J. L., Fowler, S. W., Fichez, R., & Warnau, M. (2006). Allometric relationships in the bioconcentration of heavy metals by the edible tropical clam Gafrarium tumidum. Science of the Total Environment, 366, 154–163.CrossRefGoogle Scholar
  48. Hédouin, L., Pringault, O., Metian, M., Bustamante, P., & Warnau, M. (2007). Nickel bioaccumulation in bivalves from the New Caledonia lagoon: Seawater and food exposure. Chemosphere, 66, 1449–1457.CrossRefGoogle Scholar
  49. Huanxin, W., Lejun, Z., & Presley, B. J. (2000). Bioaccumulation of heavy metals in oyster (Crassostrea virginica) tissue and shell. Environmental Geology, 39, 1216–1226.CrossRefGoogle Scholar
  50. Jimenez-Berrocoso, A., Zuluaga, M., & Elorza, J. (2004). Minor- and trace-element intra-shell variations in Santonian inoceramids (Basque-Cantabrian Basin, northern Spain): diagenetic and primary causes. Facies, 50, 35–60.CrossRefGoogle Scholar
  51. Jolliffe, I.T., (2002). Principal Component Analysis. Second edition. Springer. 487 pp.Google Scholar
  52. Kim, K.T., Kim, E.S., Cho, S.R., Park, J.K., Ra, K.T., Lee, J.M., (2010). Distribution of Heavy Metals in the Environmental Samples of the Saemangeum Coastal Area, Korea. Coastal Environmental and Ecosystem Issues of the East China Sea, 71–90.Google Scholar
  53. Koide, M., Lee, D. S., & Goldberg, E. D. (1982). Metal and transuranic records in mussel shells, byssal threads and tissues. Estuarine, Coastal and Shelf Science, 15, 679–695.CrossRefGoogle Scholar
  54. Kuisma-Kursula, P., (1999). PIXE and SEM Studies of Old Finnish and European Glass and European Oyster Ostrea edulis. University of Helsinki 41 pp.Google Scholar
  55. Leoni, L., & Sartori, F. (1997). Heavy metal and arsenic distributions in sediments of the Elba-Argentario basin, southern Tuscany, Italy. Environmental Geology, 32(2), 83–92.CrossRefGoogle Scholar
  56. Liehr, G. A., Zettler, M. L., Leipe, T., & Witt, G. (2005). The ocean quahog Arctica islandica L.: a bioindicator for contaminated sediments. Marine Biology, 147, 671–679.CrossRefGoogle Scholar
  57. Limburg, K. E. (2004). The biogeochemistry of strontium: a review of H.T. Odum’s contributions. Ecological Modeling, 178, 31–33.CrossRefGoogle Scholar
  58. Liu, X., Yan, Z., Zheng, G., Zhang, G., Wang, H., Xie, L., & Zhang, R. (2011). A possible mechanism for the formation of annual growth lines in bivalve shells. Science China. Life Sciences, 54(2), 175–180.Google Scholar
  59. Ludwig, J. A., & Reynolds, J. F. (1988). Statistical ecology: A primer on methods and computing. New York: John Wiley & Sons. 337 pp.Google Scholar
  60. Maanan, M. (2008). Heavy metal concentrations in marine molluscs from the Moroccan coastal region. Environmental Pollution, 153, 176–183.CrossRefGoogle Scholar
  61. Madkour, H. A. (2005). Distribution and relationships of heavy metals in the giant clam (Tridacna maxima) and associated sediments from different sites in the Egyptian Red Sea coast. Egyptian Journal of Aquatic Research, 31(2), 45–59.Google Scholar
  62. Maya, K., (2005). Studies on the nature and chemistry of sediments and water of Periyar and Chalakudy rivers, Kerala, India. Department of Marine Geology and Geophysics, School of Marine Sciences, Cochin University of Science and Technology, Kochi - 682 016, 160 pp.Google Scholar
  63. MHSPE. (1999). Setting integrated environmental quality standards for substances in the Netherlands. The Netherlands: Ministry of HousingSpatial Planning and Environment, The Hague.Google Scholar
  64. Moloukhia, H., & Sleem, S. (2011). Bioaccumulation, Fate and Toxicity of Two Heavy Metals Common in Industrial Wastes in Two Aquatic Molluscs. Journal of American Science, 7(8), 459–464.Google Scholar
  65. MOOPAM. (2010). Manual of oceanographic observations and pollutant analysis methods. Kuwait: Regional Organization for Protection of the Marine Environment (ROPME). 543 pp.Google Scholar
  66. Nicholas, J., Pearce, G., & Mann, V. L. (2006). Trace metal variations in the shells of Ensis siliqua record pollution and environmental conditions in the sea to the west of mainland Britain. Marine Pollution Bulletin, 52, 739–755.CrossRefGoogle Scholar
  67. NOAA, (1999). Sediment quality guideline developed for the national status and trends program. National Oceanic and Atmospheric Administration (NOAA),
  68. NYSDEC, (1999). Technical guidance for screening contaminated sediments. New York State Department of Environmental Conservation. Division of Fish, Wildlife and Marine Resources. 39 pp.Google Scholar
  69. Parizanganeh A., (2008). Grain size effect on trace metals in contaminated sediments along the Iranian coast of the Caspian Sea. Proceedings of Taal 2007, 12th World Lake Conference, 329–336.Google Scholar
  70. Pearce, N. J. G., & Mann, V. L. (2006). Trace metal variations in the shells of Ensis siliqua record pollution and environmental conditions in the sea to the west of mainland Britain. Marine Pollution Bulletin, 52, 739–755.CrossRefGoogle Scholar
  71. Pereira, E. R., Soares, B. M., Vieira, J. P., Mai, A. C. G., Picoloto, R. S., Muller, E. I., Flores, E. M. M., & Duarte, F. A. (2012). Assessment of Inorganic Contaminants in Golden Mussel (Limnoperna fortunei) in Southern Brazil. Journal of the Brazilian Chemical Society, 23(5), 846–853.CrossRefGoogle Scholar
  72. Perry, J. N. (1981). Taylor’s power law for dependence of variance on mean in animal populations. Applied Statistics, 30, 254–263.CrossRefGoogle Scholar
  73. Pourang, N., Nikouyan, A., & Dennis, J. H. (2005). Trace element concentrations in fish, surficial sediments and water from northern part of the Persian Gulf. Environmental Monitoring and Assessment, 109, 293–316.CrossRefGoogle Scholar
  74. Pourang, N., Richardson, C. A., & Mortazavi, M. S. (2010). Heavy metal concentrations in the soft tissues of swan mussel (Anodonta cygnea) and surficial sediments from Anzali wetland, Iran. Environmental Monitoring and Assessment, 163, 195–213.CrossRefGoogle Scholar
  75. Protasowicki, M., Dural, M., & Jaremek, J. (2008). Trace metals in the shells of blue mussels (Mytilus edulis) from the Poland coast of Baltic Sea. Environmental Monitoring and Assessment, 141, 329–337.CrossRefGoogle Scholar
  76. Putten, E. V., Dehairs, F., Keppens, E., & Baeyens, W. (2000). High resolution distribution of trace elements in the calcite shell layer of modern Mytilus edulis: Environmental and biological controls. Geochimica Et Cosmochimica Acta, 64(6), 997–1011.CrossRefGoogle Scholar
  77. Rainbow, P. S. (2002). Trace metal concentrations in aquatic invertebrates: why and so what? Environmental Pollution, 120, 497–507.CrossRefGoogle Scholar
  78. Ramadan, S. E., & Shata, A. (1993). Biogeochemical studies on the mollusk bivalve Anadara diluvii (Lamarck, 1805) (Pteriomorpha Arcidae). Bulletin of National Institute of Oceanography and Fisheries, 19, 145–157.Google Scholar
  79. Ravera, O., Beone, G. M., Cenci, R., & Lodigiani, P. (2003). Metal concentrations in Unio pictorum mancus (Mollusca, lamellibranchia) from of 12 Northern Italian lakes in relation to their trophic level. Journal of Limnology, 62(2), 121–138.CrossRefGoogle Scholar
  80. Ravera, O., Beone, G. M., Trincherini, P. R., & Riccardi, N. (2007). Seasonal variations in metal content of two Uniopictorum mancus (Mollusca, Unionidae) populations from two lakes of different trophic state. Journal of Limnology, 66, 28–39.Google Scholar
  81. Reyahi Bakhteyari, A., & Mortazavi, S. (2007). Measurement of Pb And Cd in the shell of Pinctada Radiata in Hendorabi Island. Pajouhesh and Sazandegi, 74, 111–117.Google Scholar
  82. Richardson, C. A., Chenery, S. R. N., & Cook, J. M. (2001). Assessing the history of trace metal (Cu, Zn, Pb) contamination in the North Sea through laser ablation ICP-MS of horse mussel, Modiolus modiolus shells. Marine Ecology Progress Series, 211, 157–167.CrossRefGoogle Scholar
  83. Richardson, C. A., Peharda, M., Kennedy, H., Kennedy, P., & Onofri, V. (2004). Age, growth rate and season of recruitment of Pinna nobilis (L) in the Croatian Adriatic determined from Mg:Ca and Sr:Ca shell profiles. Journal of Experimental Marine Biology and Ecology, 299, 1–16.CrossRefGoogle Scholar
  84. Ridgway, I. D., Richardson, C. A., Enos, E., Ungvari, Z., Austad, S. N., Philipp, E. E., & Csiszar, A. (2011). New species longevity record for the northern quahog (=hard clam), Mercenaria mercenaria. Journal of Shellfish Research, 30(1), 35–38.CrossRefGoogle Scholar
  85. ROPME. (1999). Regional report of the state of the marine environment. Kuwait: Regional Organization for the Protection of The Marine Environment (ROPME). 220 pp.Google Scholar
  86. Sarkar, S. K., Cabral, H., Chatterjee, M., Cardoso, I., Bhattacharya, A. K., Satpathy, K. K., & Alam, M. A. (2008). Biomonitoring of heavy metals using the bivalve molluscs in Sunderban mangrove wetland, northeast coast of Bay of Bengal (India): Possible risks to human health. Clean, 36(2), 187–194.Google Scholar
  87. Seixas, S., & Pierce, G. J. (2005). Vanadium, rubidium and potassium in Octopus vulgaris (Mollusca: Cephalopoda). Scientia Marina, 69(2), 215–222.CrossRefGoogle Scholar
  88. Shaw P.J.A., (2003). Multivariate statistics for the environmental sciences. Hodder-Arnold, 233 pp.Google Scholar
  89. Sokolowski, A., Fichet, D., Garcia-Meunier, P., Radenac, G., Wolowicz, M., & Blanchard, G. (2002). The relationship between metal concentrations and phenotypes in the Baltic clam Macoma balthica (L.) from the Gulf of Gdansk, southern Baltic. Chemosphere, 47, 475–484.CrossRefGoogle Scholar
  90. Southwood, T. R. E., & Henderson, P. A. (2000). Ecological Methods (3rd ed.). Oxford: Blackwell Sciences. 592 pp.Google Scholar
  91. Stanković, S., Jović, M., Milanov, R., & Joksimović, D. (2011). Trace elements concentrations (Zn, Cu, Pb, Cd, As and Hg) in the Mediterranean mussel (Mytilus galloprovincialis) and evaluation of mussel quality and possible human health risk from cultivated and wild sites of the southeastern Adriatic Sea, Montenegro mussel quality and possible human health risk from cultivated and wild sites of the southeastern Adriatic Sea, Montenegro. Journal of the Serbian Chemical Society, 76(12), 1725–1737.CrossRefGoogle Scholar
  92. Swedish EPA, (1991). Quality criteria for lakes and watercourses: A system for classification of water chemistry and sediment and organism metal concentrations [Allmänna råd 90:4]. Swedish Environmental Protection Agency, 32 pp.Google Scholar
  93. Szefer, P. (2002). Metals, Metalloids and Radionuclides in the Baltic Sea Ecosystem. Amsterdam: Elsevier Science. 764 pp.Google Scholar
  94. Tanabe, K., Sano, Y., Shirai, K., Miyaji, T., (2007). Micro-scale elemental distribution in a shell of the venerid bivalve Phacosoma japonicum. First International Scleorochronoloty Conference Abstract: 81.Google Scholar
  95. Tariq, J., Jaffar, M., & Ashraf, M. (1994). Distribution of trace metals in sediment and seawater from the continental shelf of Pakistan. Indian Journal of Marine Sciences, 23, 147–151.Google Scholar
  96. Türkmen, M., & Ciminli, C. (2007). Determination of metals in fish and mussel species by inductively coupled plasma-atomic emission spectrometry. Food Chemistry, 103(2), 670–675.CrossRefGoogle Scholar
  97. US.EIA, (2012). Country analysis briefs: Iran. U.S. Energy Information Administration (EIA) 13 pp.
  98. Usero, J., Morillo, J., & Gracia, I. (2005). Heavy metal concentrations in molluscs from the Atlantic coast of southern Spain. Chemosphere, 59, 1175–1181.CrossRefGoogle Scholar
  99. Wanamaker, A. D., Heinemeier, J., Scourse, J. D., Richardson, C. A., Butler, P. G., Eiriksson, J., & Knudsen, K. L. (2008). Very long-lived molluscs confirm 17th century AD tephra-based radiocarbon reservoir ages for north Icelandic shelf waters. Radiocarbon, 50, 399–412.Google Scholar
  100. WDOE, (1995). Sediment management standards. Olympia: Washington State Department of Ecology (Chapter 173-204-320) WAC. State of Washington. 66 pp.Google Scholar
  101. Wheeler, A. P. (1992). Mechanisms of molluscan shell formation. In E. Bonucci (Ed.), Calcification in Biological Systems. New York: CRC press. 216 pp.Google Scholar
  102. Yap, C. K., Ismail, A., Tan, S. G., & Rahim Ismail, A. (2007). The distribution of the heavy metals (Cu, Pb and Zn) in the soft and hard tissues of the green-lipped Perna viridis (Linnaeus) collected from Pasir Panjang, Peninsular Malaysia. Pertanika Journal of Tropical Agricultural Science, 30(1), 1–10.Google Scholar
  103. Zainal, K., Al-Sayed, H., Al-Madany, I., (2008). Coastal pollution in Bahrain and its management. Protecting the Gulf’s Marine Ecosystems from Pollution, 147–162.Google Scholar
  104. Zar, J. H. (1999). Biostatistical Analysis, 4th Edition, Prentice-Hall. New Jersey: Inc. Englewood Cliffs. 718 pp.Google Scholar
  105. Zhang, Z., (2009). Geochemical properties of shells of Arctica islandica (Bivalvia). implications for environmental and climatic change. PhD thesis, University of Frankfurt, 109 pp.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • N. Pourang
    • 1
  • C. A. Richardson
    • 2
  • S. R. N. Chenery
    • 3
  • H. Nasrollahzedeh
    • 4
  1. 1.Iran Fisheries Research OrganizationTehranIran
  2. 2.School of Ocean SciencesBangor UniversityMenai BridgeUK
  3. 3.British Geological SurveyNottinghamUK
  4. 4.Caspian Sea Ecology Research Center (CSERC)SariIran

Personalised recommendations