Abstract
This study aimed to evaluate the relationship between physicochemical parameters and heavy metal (Cu, Ni, Pb, and Cd) concentrations from sediment, seawater, and its accumulation in tissues of oyster species (Crassostrea madrasensis and C. gryphoides) from the three sites (Chicalim Bay (CB), Nerul Creek (NC), Chapora Bay (ChB)) along the Goa coast (India). Results showed enrichment of Cu and Ni in sediment exceeding the effect range low (ERL) level. The higher concentrations of Cu and Ni in sediments and in suspended particulate matter (SPM) from all the study sites are indicative of severe contamination of estuarine and associated habitats. Moreover, particulate Ni (at all the sites), Cu (at NC and ChB), Pb (at NC), and Cd (at CB and NC) concentrations were recorded more than its total loadings in surface sediment. Concentration of Cu and Cd in oyster tissue was several folds higher than its concentration in ambience. Further, this study showed that the levels of metal in oysters and their ambient environment were higher during the monsoon season. Hence, the consumption of oysters needs to be considered carefully with respect to the health hazards posed by the elevated levels of metal contaminants in certain seasons. The present study concludes that metals associated with the particulate matter in water column are the main source of metal accumulation in oyster. It is also suggested that concentration of metal pollutants in coastal and estuarine water bodies should be monitored regularly to ensure the acceptable limits of metal concentrations.
Similar content being viewed by others
References
Aguilar CA, Montalvo C, Rodriguez L, Ceron JG, Ceron RM (2012) American oyster (Crassostrea virginica) and sediments as a coastal zone pollution monitor by heavy metals. Int J Environ Sci Technol 9:579–586
Alagarsamy R (2006) Distribution and seasonal variation of trace metals in the surface sediments of the Mandovi estuary, west coast of India. Estuar Coast Shelf Sci 67:333–339
Alfonso JA, Handt H, Mora A, Vásquez Y, Azocar J, Marcano E (2013) Temporal distribution of heavy metal concentrations in oysters Crassostrea rhizophorae from the central Venezuelan coast. Mar Pollut Bull 73:394–398
Apeti DA, Lauenstein GG, Riedel GF (2009) Cadmium distribution in coastal sediments and mollusks of the US. Mar Pollut Bull 58:1016–1024
Balkis N, Aksu A, Okus E, Apak R (2010) Heavy metal concentrations in water, suspended matter, and sediment from Gokova Bay, Turkey. Environ Monit Assess 167(1–4):359–370
Belivermis M, Warnau M, Metian M, Oberhansli F, Teyssie JL, Lacoue-Labarthe T (2016) Limited effects of increased CO2 and temperature on metal and radionuclide bioaccumulation in a sessile invertebrate, the oyster Crassostrea gigas. ICES J Mar Sci 73(3):753–763
Birch GF, Melwani A, Lee JH, Apostolatos C (2014) The discrepancy in concentration of metals (Cu, Pb and Zn) in oyster tissue (Saccostrea glomerata) and ambient bottom sediment (Sydney estuary, Australia). Mar Pollut Bull 80:263–274
ter Braak CJF, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Section on permutation methods. Microcomputer power, Ithaca, New York
Bray DJ, Green I, Golicher D, Herbert RJH (2015) Spatial variation of trace metals within intertidal beds of native mussels (Mytilus edulis) and non-native Pacific oysters (Crassostrea gigas): implications for the food web? Hydrobiologia 757:235–249
Brewer PG, Spencer DW, Smith CL (1969) Determination of trace metals in seawater by atomic absorption spectroscopy. ASTM Special Tech Publ 443:7–77
Bruder HV, Lagarde F, Leroy MJ, Coughanowr C, Enguehard F (2002) Application of a sequential extraction procedure to study the release of elements from municipal solid waste incineration bottom ash. Anal Chim Acta 451:285–295
Bruland KW (1983) Trace elements in seawater. In: Riley JP, Chester R (eds) Chemical oceanography. Academic Press, London, pp 157–220
Burton Jr GA (2002) Sediment quality criteria in use around the world. Limnology 3(2):65–76
Caetano M, Madureira MJ, Vale C (2003) Metal remobilization during resuspension of anoxic contaminated sediment: short-term laboratory study. Water Air Soil Pollut 143:23–40
Chakraborty P, Ramteke D, Chakraborty S (2015) Geochemical partitioning of Cu and Ni in mangrove sediments: relationships with their bioavailability. Mar Pollut Bull 93:194–201
Chakraborty P, Ramteke D, Gadi SD, Bardhan P (2016) Linkage between speciation of Cd in mangrove sediment and its bioaccumulation in total soft tissue of oyster from the west coast of India. Mar Pollut Bull 106:274–282
Chapman PM, Wang F, Janssen C, Persoone G, Allen HE (1998) Ecotoxicology of metals in aquatic sediments: binding and release, bioavailability, risk assessment, and remediation. Can J Fish Aquat Sci 55:2221–2243
Cheng WW, Gobas FA (2007) Assessment of human health risks of consumption of cadmium contaminated cultured oysters. Hum Ecol Risk Assess 13(2):1–13
Cheung YH, Wong MH (1992) Trace metal contents of the pacific oyster (Crassostrea gigas) purchased from markets in Hong Kong. Environ Manag 16(6):753–761
Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth
Dassenakis M, Degaita A, Scoullos M (1995) Trace metals in sediments of a Mediterranean estuary affected by human activities (Acheloos river estuary, Greece). Sci Total Environ 168:19–31
De Mora S, Fowler SW, Wyse E, Azemard S (2004) Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf of Oman. Mar Pollut Bull 49:410–424
Depledge MH, Rainbow PS (1990) Models of regulation and accumulation of trace metals in marine invertebrates. Comp Biochem Physiol C Comp Pharmacol 97:1–7
Dessai DVG, Nayak GN (2009) Distribution and speciation of selected metals in surface sediments, from the tropical Zuari estuary, central west coast of India. Environ Monit Assess 158:117–137
Eggleton J, Thomas KV (2004) A review of factors affecting the release and bioavailability of contaminants during sediment disturbance events. Environ Int 30:973–980
European Union (2001) Commission regulation as regards heavy metals. Directive 2001/22/EC, No 466/2001
FAO (1983) Compilation of legal limits for hazardous substances in fish and fishery products. Food and agriculture Organization of the United Nations, Rome. FAO Fish Circ 464:5–100
Flora G, Gupta D, Tiwari A (2012) Toxicity of lead: a review with recent updates. Interdiscip Toxicol 5(2):47–58
Forstner U, Whittmann GTW (1981) Metal pollution in the aquatic environment. Springer-Verlag, New York
Frazier JM (1975) The dynamics of metals in the American oyster, Crassostrea virginica. I. Seasonal effects. Science 16(3):162–171
Fuad MM, Shazili NAM, Faridah M (2013) Trace metals and rare earth elements in rock oyster Saccostrea cucullata along the east coast of peninsular Malaysia. Aquat Ecosyst Health Manag 16:78–87
Gorman M (1993) Environmental hazards: marine pollution. ABC-CLIO, Santa Barbara, California
Hamad SH, Schauer JJ, Shafer MM, Al-Raheem EA, Satar H (2012) The distribution between the dissolved and the particulate forms of metals across the Tigris River, Baghdad. Iraq Sci World J 2012:1–13. https://doi.org/10.1100/2012/246059
Heidari B, Bakhtiari AR, Shirneshan G (2013) Concentrations of Cd, Cu, Pb and Zn in soft tissue of oyster (Saccostrea cucullata) collected from the Lengeh Port coast, Persian Gulf, Iran: a comparison with the permissible limits for public health. Food Chem 141:3014–3019
Huanxin W, Lejun Z, Presley BJ (2000) Bioaccumulation of heavy metals in oyster (Crassostrea virginica) tissue and shell. Environ Geol 39(11):1216–1226
Hung TC, Han BC (1990) Copper availability and assimilative capacity in sea water along the charting coastal area. Council Agri Fish ser 23:221–229
Jiann K, Santschi PH, Presley BJ (2013) Relationships between geochemical parameters (pH, DOC, SPM, EDTA concentrations) and trace metal (Cd, Co, Cu, Fe, Mn, Ni, Pb, Zn) concentrations in river waters of Texas (USA). Aquat Geochem 19:173–193
Kessarkar PM, Shynu R, Rao VP, Chong F, Narvekar T, Zhang J (2013) Geochemistry of the suspended sediment in the estuaries of the Mandovi and Zuari rivers, central west coast of India. Environ Monit Assess 185:4461–4480
Krishna Kumari LK, Kaisary S, Rodrigues V (2006) Bioaccumulation of some trace metals in the short-neck clam Paphia malabarica from Mandovi estuary, Goa. Environ Int 32:229–234
Lannig G, Flores JF, Sokolova IM (2006) Temperature-dependent stress response in oysters, Crassostrea virginica: pollution reduced temperature tolerance in oysters. Aquat Toxicol 79:278–287
Lee JH, Richards RG, Birch GF (2013) what is the role of sediment resuspension in the bioaccumulation of heavy metals in oysters? 20th international congress on modelling and simulation. Adelaide, Australia, pp 1742–1748
Leps J, Smilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge, UK
Madhupratap M, Nair KNV, Gopalakrishnan TC, Haridas P, Nair KKC, Venugopal P, Gauns MU (2001) Arabian Sea oceanography and fisheries of the west coast of India. Curr Sci 81(4):355–361
National aquaculture sector overview-India (2016) Food and agriculture organization of the United Nations. http://www.fao.org/fishery/countrysector/naso_india/en. Accessed 2 March 2016
Nelson A, Donkin P (1985) Process of bioaccumulation: the importance of chemical speciation. Mar Pollut Bull 16:164–169
O’Connor TP (2001) National distribution of chemical concentrations in mussels and oysters in the US. Mar Environ Res 53:117–143
Paez-Osuna F, Osuna-Martınez CC (2015) Bioavailability of cadmium, copper, mercury, lead, and zinc in subtropical coastal lagoons from the southeast gulf of California using mangrove oysters (Crassostrea corteziensis and Crassostrea palmula). Arch Environ Contam Toxicol 68:305–316
Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford
Peakall D, Burger J (2003) Methodologies for assessing exposure to metals: speciation, bioavailability of metals, and ecological host factors. Ecotoxicol Environ Saf 56:110–121
Pekey H (2006) The distribution and sources of heavy metals in Izmit Bay surface sediments affected by a polluted stream. Mar Pollut Bull 52:1197–1208
Rainbow PS (1995) Biomonitoring of heavy metal availability in the marine environment. Mar Pollut Bull 31(4–12):183–192
Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Environ Pollut 120:497–507
Rainbow PS, Philips DJH, Depledge MH (1990) The significance of trace metal concentrations in marine invertebrates a need for laboratory investigation of accumulation strategies. Mar Pollut Bull 21:321–324
Rao VP, Shynu R, Kessarkar PM, Sundar D, Michael GS, Narvekar T, Blossom V, Mehra P (2011) Suspended sediment dynamics on a seasonal scale in the Mandovi and Zuari estuaries, central west coast of India. Estuar Coast Shelf Sci 91:78–86
Rath P, Panda UC, Bhatta D, Sahu KC (2009) Use of sequential leaching, mineralogy, morphology and multivariate statistical technique for quantifying metal pollution in highly polluted aquatic sediments – a case study: Brahamani and Nandira rivers, India. J Hazard Mater 163:632–644
Reddy NPC, Rao BP, Rao KM, Rao VS (1994) Seasonal changes in suspended sediment load in the Gautami-Godavari estuary. Mahasagar 27(1):47–53
Sarkar SK, Bhattacharya B, Debnath S (1994) The suitability of tropical marine bivalves as biomonitors of heavy metals in deltaic Sundarbans, north-East India. Chemosphere 29(4):759–770
Schoellhamer DH (1995) Sediment resuspension mechanisms in old Tampa Bay, Florida. Estuar Coast Shelf Sci 40:603–620
Shynu R, Rao VP, Parthiban G, Balakrishnan S, Narvekar T, Kessarkar PM (2013) REE in suspended particulate matter and sediment of the Zuari estuary and adjacent shelf, western India: influence of mining and estuarine turbidity. Mar Geol 346:326–342
Shynu R, Rao VP, Sarma VVSS, Kessarkar PM, Mani Murali R (2015) Sources and fate of organic matter in suspended and bottom sediments of the Mandovi and Zuari estuaries, western India. Curr Sci 108(2):226–238
STATISTICA (data analysis software system) (2007) StatSoft, Inc version 8.0
Tait RV, Dipper F (1998) Elements of Marine Ecology, Butterworth-Heinemann, Fourth edition, pp 453
Turkmen A, Turkmen M, Tepe Y (2005) Biomonitoring of heavy metals from Iskenderun Bay using two bivalve species Chama pacifica Broderip, 1834 and Ostrea stentina Payraudeau, 1826. Turk J Fish Aquat Sci 5:107–111
UNESCO (1994) Protocols for the Joint Global Ocean Flux Study. pp 97–128
USFDA (1993) Food and drug administration, Guidance document for nickel in shell fish. DHHS/PHS/ FDA/CFSAN/office of seafood, Washington D.C
Vazquez-Boucard C, Anguiano-Vega G, Mercier L, del Castillo ER (2014) Pesticide residues, heavy metals, and DNA damage in sentinel oysters Crassostrea gigas from Sinaloa and Sonora, Mexico. J Toxicol Environ Health A 77:169–176
Veerasingam S, Vethamony P, Mani Murali R, Fernandes B (2015) Depositional record of trace metals and degree of contamination in core sediments from the Mandovi estuarine mangrove ecosystem, west coast of India. Mar Pollut Bull 91:362–367
Viles H, Spencer T (1995) Coastal problems: geomorphology, ecology and society at the coast. Edward Arnold, Great Britain, p 350
Violante A, Cozzolino V, Perelomov L, Caporale AG, Pigna M (2010) Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Sci Plant Nutr 10(3):268–292
Wang WX, Fisher NS (1999) Assimilation efficiencies of chemical contaminants in aquatic invertebrates: a synthesis. Environ Toxicol Chem 18(9):2034–2045
Xu W, Li X, Wai OWH, Huang W, Yan W (2015) Remobilization of trace metals from contaminated marine sediment in a simulated dynamic environment. Environ Sci Pollut Res 22:19905–19911
Yap CK, Mohd Ruszaidi S, Cheng WH (2010) Different tissues of rock oyster Saccostrea cucullata as biomonitors of trace metal bioavailabilities in the Penang coastal waters, Malaysia. Res J Chem Environ 14(3):17–21
Yu XJ, Pan K, Liu F, Yan Y, Wang WX (2013) Spatial variation and subcellular binding of metals in oysters from a large estuary in China. Mar Pollut Bull 70:274–280
Acknowledgements
The authors are thankful to S.W.A. Naqvi, Former Director, CSIR-NIO for his encouragement and providing all facilities to carry out this work. Authors are also grateful to the Dr. B. N. Nath, Dr. J. N. Pattan, Mr. D. Ray, and Dr. A. Ram (RC-NIO, Mumbai) for providing the chemicals and lab facilities for sample analysis. The first author would like to acknowledge CSIR, New Delhi, for providing the fellowship to carry out the Ph.D. research. This is NIO contribution no. 6219.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Philippe Garrigues
Electronic supplementary material
ESM 1
(DOCX 227 kb)
Rights and permissions
About this article
Cite this article
Shenai-Tirodkar, P., Gauns, M., Kumar, G. et al. Seasonal variations and relationships between environmental parameters and heavy metal concentrations in tissues of Crassostrea species and in its ambience from the tropical estuaries. Environ Sci Pollut Res 25, 20930–20945 (2018). https://doi.org/10.1007/s11356-018-2258-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-2258-x