Skip to main content
Log in

Assessment of trace metal concentrations and human health risk in clam (Tapes decussatus) and mussel (Mytilus galloprovincialis) from the Homa Lagoon (Eastern Aegean Sea)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Seasonal variations of trace metal concentrations (Hg, Cd, Pb, Cr, Zn, and Cu) were investigated in the hepatopancreas and soft tissues (remaining parts of bivalves such as gill, mantle, foot, and muscle) of Tapes decussatus and Mytilus galloprovincialis from the Homa Lagoon. The highest metal concentrations were recorded frequently in February and July in M. galloprovincialis and T. decussatus, respectively. Trace metal levels (except Zn) in the hepatopancreas were higher than those in soft tissue for both bivalves. The results showed that the mean concentrations of Hg, Cd, and Zn for M. galloprovincialis were higher compared to T. decussatus in both tissues. The metal concentrations in both bivalves from the Homa Lagoon were generally below the values of provisional tolerable weekly intake (PTWI) estimates, in terms of human health risk. According to hazard quotient (HQ), Cr values for both species and Cd values for only M. galloprovincialis were found greater than one. Also, total hazard index (THI) values were greater than one in both bivalves, having a potential risk for consumers.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ali M, Taylor A (2010) The effect of salinity and temperature on the uptake of cadmium and zinc by the common blue mussel, Mytilus edulis with some notes on their survival. Mesopot J Mar Sci 25(1):11–30

    Google Scholar 

  • Allison N, Millward GE, Jones MB (1998) Particle processing by Mytilus edulis: effects on bioavailability of metals. J Exp Mar Biol Ecol 222(1):149–162. doi:10.1016/S0022-0981(97)00136-6

    Article  CAS  Google Scholar 

  • Atılgan I, Egemen Ö (2001) A comparative investigation on the levels of carbon, flammable substance and some heavy metals (Cu,Zn) accumulated in sediment of Güllük and Homa Lagoons. Ege J Fish Aqua Sci 18(1–2):225–232

    Google Scholar 

  • ATSDR (2016) Minimal risk levels (MRLs), March 2016. http://www.atsdr.cdc.gov/mrls/mrllist.asp (accessed 25th April 2016)

  • Bebianno MJ, Serafim MA (1998) Comparison of metallothionein induction in response to cadmium in the gills of the bivalve molluscs Mytilus galloprovincialis and Ruditapes decussatus. Sci Total Environ 214(1):123–131. doi:10.1016/S0048-9697(98)00059-X

    Article  CAS  Google Scholar 

  • Bebianno MJ, Serafim MA (2003) Variation of metal and metallothionein concentrations in a natural population of Ruditapes decussatus. Arch Environ Con Tox 44(1):53–66. doi:10.1007/s00244-002-2004-7

    Article  CAS  Google Scholar 

  • Beiras R, Albentosa M (2004) Inhibition of embryo development of the commercial bivalves Ruditapes decussatus and Mytilus galloprovincialis by trace metals; implications for the implementation of seawater quality criteria. Aquaculture 230(1):205–213. doi:10.1016/S0044-8486(03)00432-0

    Article  Google Scholar 

  • Belabed BE, Laffray X, Dhib A, Fertouna-Belakhal M, Turki S, Aleya L (2013) Factors contributing to heavy metal accumulation in sediments and in the intertidal mussel Perna perna in the Gulf of Annaba (Algeria). Mar Pollut Bull 74(1):477–489. doi:10.1016/j.marpolbul.2013.06.004

    Article  CAS  Google Scholar 

  • Branch GM, Steffani NC (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). J Exp Mar Biol Ecol 300:189–215. doi:10.1016/j.jembe.2003.12.007

    Article  Google Scholar 

  • Breber P (1985) On-growing of the carpet shell clam (Tapes decussatus (L.)): two years’ experience in Venice Lagoon. Aquaculture 44:51–56. doi:10.1016/0044-8486(85)90041-9

    Article  Google Scholar 

  • Caçador I, Costa JL, Duarte B, Silva G, Medeiros JP, Azeda C, Castro N, Freitas J, Pedro S, Almeida PR, Cabral H, Costa MJ (2012) Macroinvertebrates and fishes as biomonitors of heavy metal concentration in the Seixal Bay (Tagus estuary): which species perform better? Ecol Indic 19:184–190. doi:10.1016/j.ecolind.2011.09.007

    Article  Google Scholar 

  • Catsiki VA, Florou H (2006) Study on the behavior of the heavy metals Cu, Cr, Ni, Zn, Fe, Mn and 137Cs in an estuarine ecosystem using Mytilus galloprovincialis as a bioindicator species: the case of Thermaikos gulf, Greece. J Environ Radioactiv 86(1):31–44. doi:10.1016/j.jenvrad.2005.07.005

    Article  CAS  Google Scholar 

  • Chapman PM, Wang F (2001) Assessing sediment contamination in estuaries. Environ Toxicol Chem 20:3–22. doi:10.1002/etc.5620200102

    Article  CAS  Google Scholar 

  • Cravo A, Bebianno MJ, Foster P (2004) Partitioning of trace metals between soft tissues and shells of Patella aspera. Environ Int 30:87–98. doi:10.1016/S0160-4120(03)00154-5

    Article  CAS  Google Scholar 

  • Cravo A, Pereira C, Gomes T, Cardoso C, Serafim A, Almeida C, Rocha T, Lopes B, Company R, Madeiros A, Norberto R, Pereira R, Araujo O, Bebianno MJ (2012) A multibiomarker approach in the clam Ruditapes decussatus to assess the impact of pollution in the Ria Formosa lagoon, south coast of Portugal. Mar Environ Res 75:23–34. doi:10.1016/j.marenvres.2011.09.012

    Article  CAS  Google Scholar 

  • Deudero S, Box A, March D, Valencia JM, Grau AM, Tintore J, Benedicto J (2007) Temporal trends of metals in benthic invertebrate species from the Balearic Islands, western Mediterranean. Mar Pollut Bull 54(9):1545–1558. doi:10.1016/j.marpolbul.2007.05.012

    Article  CAS  Google Scholar 

  • Dora EÇ, Sunlu U, Ergen Z (2007) Heavy metal concentrations in Hediste diversicolor (polychaete) and sediments from Homa Lagoon (Izmir Bay-Turkey). CIESM 38th meeting:253

  • Eisler R (2000) Handbook of chemical risk assessment: health hazards to humans, plants and animals. Lewis Publishers, Florida

    Book  Google Scholar 

  • El Nemr A, Khaled A, Moneer AA, El Sikaily A (2012) Risk probability due to heavy metals in bivalve from Egyptian Mediterranean coast. Egypt J Aqua Res 38(2):67–75. doi:10.1016/j.ejar.2012.11.001

    Article  Google Scholar 

  • El-Sikaily A, Khaled A, El Nemr A (2004) Heavy metals monitoring using bivalves from Mediterranean Sea and Red Sea. Environ Monit Asses 98:41–58. doi:10.1023/B:EMAS.0000038178.98985.5d

    Article  CAS  Google Scholar 

  • European Union (2000) Directive 2000/60/EC of the European Parliament and of the council of 23 October 2000 establishing a framework for community action in the field of water policy. Official Journal L 327

  • FAO (2011) FAOSTAT, Food Supply-Livestock and Fish Primary Equivalent http://fenix.fao.org/faostat/beta/en/#data/CL Accessed 18 October 2016

  • FAO/WHO (2004) Summary of evaluations performed by the joint FAO/WHO expert committee on food additives (JECFA 1956–2003). ILSI Press International Life Sciences Institute, Washington

  • FAO/WHO (2007) Summary of evaluations performed by the joint FAO/WHO expert committee on food additives (JECFA 1956–2007) (first through 68th meetings). Food and Agriculture Organization of the United States and the World Health Organization. ILSI Press International Life Sciences Institute, Washington

  • FAO/WHO (2010) Summary of evaluations performed by the joint FAO/WHO expert committee on food additives. Seventy-third meeting, Geneva, 8–17 June 2010

  • Fattorini D, Notti A, Di Mento R, Cicero AM, Gabellini M, Russo A, Regoli F (2008) Seasonal, spatial and inter-annual variations of trace metals in mussels from the Adriatic Sea: a regional gradient for arsenic and implications for monitoring the impact of off-shore activities. Chemosphere 72(10):1524–1533. doi:10.1016/j.chemosphere.2008.04.071

    Article  CAS  Google Scholar 

  • Fernandes C, Fontainhas-Fernandes A, Cabral D, Salgado MA (2008) Heavy metals in water, sediment and tissues of Liza saliens from Esmoriz-Paramos lagoon, Portugal. Environ Monit Asses 136:267–275. doi:10.1007/s10661-007-9682-6

    Article  CAS  Google Scholar 

  • Giarratano E, Amin OA (2010) Heavy metals monitoring in the southernmost mussel farm of the world (Beagle Channel, Argentina). Ecotox Environ Safe 73(6):1378–1384. doi:10.1016/j.ecoenv. 2010.06.023

    Article  CAS  Google Scholar 

  • Guerra K, Konz J, Lisi K, Neebrem C (2010) Exposure factors handbook. USEPA, Washington DC

    Google Scholar 

  • Irato P, Santovito G, Cassini A, Piccinni E, Albergoni V (2003) Metal accumulation and binding protein induction in Mytilus galloprovincialis, Scapharca inaequivalvis, and Tapes philippinarum from the lagoon of Venice. Arch Environ Con Tox 44:476–484. doi:10.1007/s00244-002-1262-8

    Article  CAS  Google Scholar 

  • Ivanković D, Pavičić J, Erk M, Filipović-Marijić V, Raspor B (2005) Evaluation of the Mytilus galloprovincialis Lam. digestive gland metallothionein as a biomarker in a long-term field study: seasonal and spatial variability. Mar Pollut Bull 50(11):1303–1313. doi:10.1016/j.marpolbul.2005.04.039

    Article  Google Scholar 

  • Joksimovic D, Tomic I, Stankovic AR, Jovic M, Stankovic S (2011) Trace metal concentrations in Mediterranean blue mussel and surface sediments and evaluation of the mussels quality and possible risks of high human consumption. Food Chem 127(2):632–637. doi:10.1016/j.foodchem.2011.01.057

    Article  CAS  Google Scholar 

  • Kennedy PC (1986) The use of molluscs for monitoring trace elements in the marine environment in New Zealand 1. The contribution of ingested sediment to the trace element concentrations in New Zealand molluscs. New Zeal J Mar Fresh 20:627–640. doi:10.1080/00288330.1986.9516183

    Article  CAS  Google Scholar 

  • Kucuksezgin F, Kacar A, Kucuksezgin G, Uluturhan E (2010) Monitoring metal contamination levels and fecal pollution in clam (Tapes decussatus) collected from Izmir Bay (Turkey). Environ Monit Asses 162(1–4):407–415. doi:10.1007/s10661-009-0805-0

    Article  CAS  Google Scholar 

  • Kucuksezgin F, Kayatekin BM, Uluturhan E, Uysal N, Acikgoz O, Gonenc S (2008) Preliminary investigation of sensitive biomarkers of trace metal pollution in mussel (Mytilus galloprovincialis) from Izmir Bay (Turkey). Environ Monit Asses 141(1–3):339–345. doi:10.1007/s10661-007-9900-2

    Article  CAS  Google Scholar 

  • Kucuksezgin F, Kontas A, Uluturhan E (2011) Evalutions of heavy metal pollution in sediment and Mullus barbatus from the Izmir Bay (eastern Aegean) during 1997-2009. Mar Pollut Bull 62:1562–1571. doi:10.1016/j.marpolbul.2011.05.012

    Article  CAS  Google Scholar 

  • Kumar V, Sinha AK, Rodrigues PP, Mubiana VK, Blust R, De Boeck G (2015) Linking environmental heavy metal concentrations and salinity gradients with metal accumulation and their effects: a case study in 3 mussel species of Vitória estuary and Espírito Santo bay, Southeast Brazil. Sci Total Environ 523:1–15

    Article  CAS  Google Scholar 

  • Maanan M (2008) Heavy metal concentrations in marine molluscs from the Moroccan coastal region. Environ Pollut 153(1):176–183. doi:10.1016/j.envpol.2007.07.024

    Article  CAS  Google Scholar 

  • María-Cervantes A, Jiménez-Cárceles FJ, Álvarez-Rogel J (2009) As, Cd, Cu, Mn, Pb, and Zn contents in sediments and mollusks (Hexaplex trunculus and Tapes decussatus) from coastal zones of a Mediterranean lagoon (Mar Menor, SE Spain) affected by mining wastes. Water Air Soil Pollut 200:289–304. doi:10.1007/s11270-008-9913-7

    Article  Google Scholar 

  • Marsden JD, Smith BD, Rainbow PS (2014) Effects of environmental and physiological variables on the accumulated concentrations of trace metals in the New Zealand cockle Austrovenus stutchburyi. Sci Total Environ 470-471:324–339. doi:10.1016/j.scitotenv.2013.09.085

    Article  CAS  Google Scholar 

  • Mertz W (1992) Chromium: history and nutritional importance. Biol Trace Elem Res 132:3–8. doi:10.1007/BF02784581

    Article  Google Scholar 

  • Mordoğan H, Yaramaz Ö, Alpbaz A (1990) Homa dalyanı sedimentlerinde bazı ağır metallerin (Fe, Ni, Co, Mn, Sb) derişimlerinin araştırılması. Ege J Fish Aqua Sci 8(29–30):44–50

    Google Scholar 

  • Najdek M, Sapunar J (1987) Total and methyl-mercury content in bivalves, Mytilus galloprovincialis Lamarck and Ostrea edulis Linnaeus: relationship of biochemical composition and body size. B Environ Contam Tox 39(1):56–62. doi:10.1007/BF01691789

    Article  CAS  Google Scholar 

  • Nesto N, Romano S, Moschino V, Mauri M, Da Ros L (2007) Bioaccumulation and biomarker responses of trace metals and micro-organic pollutants in mussels and fish from the lagoon of Venice, Italy. Mar Pollut Bull 55(10):469–484. doi:10.1016/j. marpolbul.2007.09.009

    Article  CAS  Google Scholar 

  • Parlak H, Çakır A, Boyacıoğlu M, Çakal Arslan Ö (2006) Heavy metal deposition in sediments from the delta of the Gediz River (western Turkey): a preliminary study. Ege J Fish Aqua Sci 23(3–4):445–448

    Google Scholar 

  • Pereira P, Raimundo J, Vale C, Kadar E (2009) Metal concentrations in digestive gland and mantle of Sepia officinalis from two coastal lagoons of Portugal. Sci Total Environ 407:1080–1088. doi:10.1016/j.scitotenv.2008.10.023

    Article  CAS  Google Scholar 

  • Pérez-Ruzafa A, Marcos C, Pérez-Ruzafa IM, Pérez-Marcos M (2011) Coastal lagoons: “transitional ecosystems” between transitional and coastal waters. J Coastal Conserv 15(3):369–392. doi:10.1007/s11852-010-0095-2

    Article  Google Scholar 

  • Phillips DJH (1977) Effects of salinity on the net uptake of zinc by the common mussel Mytilus edulis. Mar Biol 41:79–88

    Article  CAS  Google Scholar 

  • Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Env Poll 120:497–507. doi:10.1016/S0269-7491(02)00238-5

    Article  CAS  Google Scholar 

  • Rainbow PS, Philips DJH (1993) Cosmopolitan bioindicators of trace metals. Mar Pollut Bull 26:593–601. doi:10.1016/0025-326X(93)90497-8

    Article  CAS  Google Scholar 

  • Regoli F, Orlando E (1994) Seasonal variation of trace metal concentrations in the digestive gland of the Mediterranean mussel Mytilus galloprovincialis: comparison between a polluted and a non-polluted site. Arch Environ Con Tox 27(1):36–43. doi:10.1007/BF00203885

    Article  CAS  Google Scholar 

  • Richir J, Gobert S (2014) The effect of size, weight, body compartment, sex and reproductive status on the bioaccumulation of 19 trace elements in rope-grown Mytilus galloprovincialis. Ecol Indic 36:33–47. doi:10.1016/j.ecolind.2013.06.021

    Article  CAS  Google Scholar 

  • Roméo M, Frasila C, Gnassia-Barelli M, Damiens G, Micu D, Mustata G (2005) Biomonitoring of trace metals in the Black Sea (Romania) using mussels Mytilus galloprovincialis. Water Res 39:596–604. doi:10.1016/j.watres.2004.09.026

    Article  Google Scholar 

  • Scudiero R, Cretì P, Trinchella F, Esposito MG (2014) Evaluation of cadmium, lead and metallothionein contents in the tissues of mussels Mytilus galloprovincialis from the Campania coast (Italy): levels and seasonal trends. C R Biol 337(7):451–458. doi:10.1016/j.crvi.2014.05.003

    Article  Google Scholar 

  • Serdar S, Lök A, Köse A, Yildiz H, Acarli S, Goulletquer P (2007) Growth and survival rates of carpet shell clam (Tapes decussatus Linnaeus, 1758) using various culture methods in Sufa (Homa) Lagoon, Izmir, Turkey. Aquac Eng 37:89–99. doi:10.1016/j.aquaeng.2007.02.004

    Article  Google Scholar 

  • Sokolowski A, Bawazir AS, Wolowicz M (2004) Trace metals in the brown mussel Perna perna from the coastal waters off Yemen (Gulf of Aden): how concentrations are affected by weight, sex, and seasonal cycle. Arch Environ Con Tox 46(1):67–80. doi:10.1007/s00244-003-2164-0

    Article  CAS  Google Scholar 

  • Sridhara Chary N, Kamala CT, Samuel Suman Raj D (2008) Assessing risk of heavy metals from consuming food grown on sewage irrigated soils and food chain transfer. Ecotox Environ Safe 69(3):513–524. doi:10.1016/j.ecoenv.2007.04.013

    Article  Google Scholar 

  • Sunlu U, Egemen Ö (1998) Homa Dalyanı ve İzmir Körfezi’nin (Ege Denizi) farklı bölgelerindeki kirlenme durumu ile bazı ekonomik balık türlerinde ağır metal düzeylerinin araştırılması. Ege J Fish Aqua Sci 15(3–4):241–261

    Google Scholar 

  • Szefer P (1986) Some metals in benthic invertebrates in Gdansk Bay. Mar Pollut Bull 17:503–507. doi:10.1016/0025-326X(86)90639-9

    Article  CAS  Google Scholar 

  • Szefer P, Kim CK, Kim EH, Lee CB (2004) Distribution and coassociations of trace elements in soft tissue and byssus of Mytilus galloprovincialis relative to the surrounding seawater and suspended matter of the southern part of the Korean Peninsula. Environ Pollut 106:299–314. doi:10.1016/j.envpol.2003.10.012

    Article  Google Scholar 

  • Uluturhan E, Kontas A, Can E (2011) Sediment concentrations of heavy metals in the Homa Lagoon (eastern Aegean Sea): assessment of contamination and ecological risks. Mar Pollut Bull 62:1989–1997. doi:10.1016/j.marpolbul.2011.06.019

    Article  CAS  Google Scholar 

  • UNEP (1982) Reference methods for marine pollution studies, 14

  • UNEP (1984) Determination of total Cd, Zn, Pb and Cu in selected marine organisms by flameless AAS, vol. 11

  • USEPA (2010) Risk-based concentration table. Philadelphia: United States Environmental Protection Agency, Washington DC

  • USEPA (2013) Reference Dose (RfD) description and using health risk assessments, Background document 1A, integrated risk information system (IRIS) United States Environmental Protection Agency, Washington DC

  • Usero J, Gonzalez-Regalado E, Gracia I (1997) Trace metals in the bivalve molluscs Ruditapes decussatus and Ruditapes philippinarum from the Atlantic coast of southern Spain. Environ Int 23(3):291–298. doi:10.1016/S0160-4120(97)00030-5

    Article  CAS  Google Scholar 

  • Válega M, Lillebo A, Pereira M, Cacador I, Duarte A, Pardal M (2008) Mercury in salt marshes ecosystems: Halimione portulacoides as biomonitor. Chemosphere 73:1224–1229. doi:10.1016/j.chemosphere.2008.07.053

    Article  Google Scholar 

  • Viaroli P, Lasserre P, Campostrini P (2007) Lagoons and coastal wetlands: preface. Hydrobiologia 577:1–3. doi:10.1007/s10750-006-0412-9

    Article  Google Scholar 

  • Vlahogianni T, Dassenakis M, Scoullos MJ, Valavanidis A (2007) Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals’ pollution in coastal areas from the Saronikos Gulf of Greece. Mar Pollut Bull 54(9):1361–1371. doi:10.1016/j.marpolbul.2007.05.018

    Article  CAS  Google Scholar 

  • Wright DA, Welbourn P (2002) Environmental toxicology. Cambridge environmental chemistry series / 11. Cambridge University Press, New York

    Google Scholar 

Download references

Acknowledgements

This research was funded by the Department of Scientific Research Projects of Dokuz Eylül University (project no: 2014.KB.FEN.004). Grateful thanks to especially our colleagues for their support in the field and in the laboratory. This article has been prepared within the context of Master Thesis studies of Mustafa Bilgin.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Esin Uluturhan-Suzer.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bilgin, M., Uluturhan-Suzer, E. Assessment of trace metal concentrations and human health risk in clam (Tapes decussatus) and mussel (Mytilus galloprovincialis) from the Homa Lagoon (Eastern Aegean Sea). Environ Sci Pollut Res 24, 4174–4184 (2017). https://doi.org/10.1007/s11356-016-8163-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-8163-2

Keywords

Navigation