Abstract
Monitoring heavy metal contaminants in fish is important for the assessment of environmental quality as well as food safety. In this study, European eel samples were collected from Lake Köyceğiz and Lake Võrtsjärv in 2017 and 2018. The concentrations of Mn, Cd, Zn, Pb, and Cu metals were measured by using GF-AAS in four selected tissues of eel, including liver, gill, skin, and muscle in both lakes. The pollution index (Pi, MPI) values were calculated for both lakes and the health risk for consumers was assessed for both adults and children in Turkey and Estonia. The estimated weekly intake (EWI), hazard index (HI), and lifetime cancer risk values (CRs) for the metals were calculated for both lakes. According to the results of this study, a significant difference was determined between the metal concentrations (especially Cu, Cd, and Pb) in the tissues of the eel samples taken from the two lakes. These results show that besides the pollution levels in the aquatic environment, physiological needs and metabolic activities in different habitats have a significant effect on metal accumulation in eels. In addition, HI was found to be < 1 for both adult and child consumers in both lakes, which indicates that consumers would not experience non-carcinogenic health effects. However, the values of CR for Pb and Cd were found negligible in Lake Köyceğiz, while the CR value for Pb was found to be very close to the danger limits in Lake Võrtsjärv.
Similar content being viewed by others
Data availability
All data obtained during this study are included in this published article.
References
Ahmed ASS, Rahman M, Sultana SSM, Babu OF, Sarker MSI (2019) Bioaccumulation and heavy metal concentration in tissues of some commercial fishes from the Meghna River Estuary in Bangladesh and human health implications. Mar Pollut Bull 145:436–447
Akter M, Zakir HM, Sharmin S, Quadir QF, Mehrin S (2020) Heavy metal bioaccumulation pattern in edible tissues of different farmed fishes of mymensingh area, Bangladesh, and health risk assessment. Adv Res 21(4):44–55
Aytekin T, Kargın D, Çoğun HY, Temiz Ö, Varkal HS, Kargın F (2019) Accumulation and health risk assessment of heavy metals in tissues of the shrimp and fish species from the Yumurtalik Coast of Iskenderun Gulf, Turkey. Heliyon 5(8):e02131
Batista BL, Nacano LR, Freitas R, Oliveira-Souza VC, Barbosa F (2012) Determination of essential (Ca, Fe, I, K, Mo) and toxic elements (Hg, Pb) in Brazilian rice grains and estimation of reference daily intake. Food Nutr Sci 3(1):129–134
Batty J, Pain D, Caurant F (1996) Metal concerations in ells Anguilla anguilla from the Camargue region of France. Elsevier Biol Conserv 76:17–23
Belpaire C, Goemans G (2007) The European eel (Anguilla anguilla), a rapporteur of the chemical status for the water framework directive ?. Vie et Milieu / Life & Environment, Observatoire Océanologique - Laboratoire Arago, pp 235–252. ffhal-03234845f
Bernotas P, Öğlü B, Nõges P (2020) How do environmental factors affect the yield of European eel (Anguilla anguilla) in a restocked population? Fish Res 230(2020):105649
Bordajandi LR, Gomez G, Fernandez MA, Abad E, River J, Gonzalez MJ (2003) Study on PCBs, PCDD/Fs, organochlorine pesticides, heavy metals and arsenic content in freshwater species from the river Turia (Spain). Chemosphere 53:163–171
Byer JD, Lebeuf M, Trottier S, Raach M, Alaee M et al (2015) Trends of persistent organic pollutants in American eel (Anguilla rostrata) from eastern Lake Ontario, Canada, and their potential effects on recruitment. Sci Total Environ 529:231–242
Carrasco L, Barata C, Garcia-Berthou E (2011) Patterns of mercury and methylmercury bioaccumulation in fish species downstream of a long-term mercury-contaminated site in the lower Ebro River (NE Spain). Chemosphere 84(2011):1642–1649
Commission European (2000) Directive 2000/60/EC of the European Parliament and of the Council establishing a framework for community action in the field of water policy. Of J Eueanr Union L 327:1–72
Chiesa LM, Emanuela Z, Maria N, Sara P, Enrica F et al (2019) Food risk characterization from exposure to persistent organic pollutants and metals contaminating eels from an Italian lake. Food Addit Contam Part A 36(5):779–788
Claveau J, Monperrus M, Jarry M, Pinaly H, Baudrimonth M et al (2015) Spatial and seasonal variations of methylmercury in European glass eels (Anguilla anguilla) in the Adour estuary (France) and relation to their migratory behaviour. Environ Sci Pollut Res 22:10721–10732
Dehkordi S, Fallah AA, Nematollahi A (2010) Arsenic and mercury in commercially valuable fish species from the Persian Gulf: influence of season and habitat. Food Chem Toxicol 48:2945–2950
Dekker W (2016) Management of the eel is slipping through our hands! Distribute control and orchestrate national protection. ICES J Mar Sci 73(10):2442–2452
Durrieu G, Maury-Brachet R, Girardin M, Rochard E, Boudou A (2005) Contamination by heavy metals (Cd, Zn, Cu, and Hg) of eight fish species in the Gironde estuary (France). Estuaries 28:581–591
Eira C, Torres J, Miquel J, Vaqueiro J, Soares AMVM, Vingada J (2009) Trace element concentrations in Proteocephalus macrocephalus (Cestoda) and Anguillicola crassus (Nematoda) in comparison to their fish host, Anguilla anguilla in Ria de Aveiro, Portuga. Sci Total Environ 407:991–998
EPA (2000) Guidance for assessing chemical contaminant data for use in fish advisories, volume II. Risk assessment and fish consumption limits. EPA 823-B-00–008. United States Environmental Protection Agency, Washington, DC
EPA (2008) Child-specific exposure factors handbook. EPA/600/R-06/096F. National Center for Environmental Assessment Office of Research and Development, Washington, DC
EPA (2010) Risk-based concentration table. United States Environmental Protection Agency, Washington, DC
EPA (2019) Regional screening levels (RSLs) – equations. https://www.epa.gov/risk/regional-screening-levels-rsls-equations
EUROFISH International Organisation (2017) Market Prospects for Aquaculture Species
FAO (2008) The state of world fisheries and aquaculture. Food and Agriculture Organization of the United Nations, Rome
FAO/WHO (2006) Evaluation of certain contaminants in food: sixty-fourth report of the joint FAO/WHO expert committee on food additives. WHO Technical Report Series. No. 930. WHO, Geneva
Freese M, Sühring R, Pohlmann JD, Wolschke H, Magath V et al (2016) A question of origin: dioxin-like PCBs and their relevance in stock management of European eels. Ecotoxicology 25:41–55
Geeraerts C, Belpaire C (2010) The effects of contaminants in European eel: a review. Ecotoxicology 19:239–266
Genç TO, Yılmaz F (2017) Metal accumulations in water, sediment, crab (callinectes sapidus) and two fish species (Mugil cephalus and Anguilla anguilla) from the Köyceğiz Lagoon System–Turkey: an index analysis approach. Bull Environ Contam Toxicol 99:173–181
Henry F, Amara R, Courcot L, Lacouture D, Bertho ML (2004) Heavy metals in four fish species from the French coast of the Eastern English Channel and Southern Bight of the North Sea. Environ Int 30:675–683
Hwang DW, Kim SS, Kim SG, Kim DS, Kim TH (2017) Concentrations of heavy metals in marine wild fishes captured from the southern sea of Korea and associated health risk assessments. Ocean Sci J 52:527–536
Jia Y, Wang L, Qu Z (2017) Effects on heavy metal accumulation in freshwater fishes: species, tissues, and sizes. Environ Sci Pollut Res 24:9379–9386
Keshavarzi B, Hassanaghaei M, Moore F, Mehr MR, Soltanian S et al (2018) Heavy metal contamination and health risk assessment in three commercial fish species in the Persian Gulf. Mar Pollut Bull 129:245–252
Kojadinovic J, Potier M, Corre ML, Cosson RP, Bustamante P (2007) Bioaccumulation of trace elements in pelagic fish from the Western Indian Ocean. Environ Pollut 146(2):548–566
Kortei NK, Heymann ME, Essuman EK, Kpodo FM, Akonor PT et al (2020) Health risk assessment and levels of toxic metals in fishes (Oreochromis noliticus and Clarias anguillaris) from Ankobrah and Pra basins: impact of illegal mining activities on food safety. Toxicol Rep 7:360–369
Kosker AR (2020) Metal and fatty acid levels of some commercially important marine species from the northeastern Mediterranean: benefits and health risk estimation. Environ Monit Assess 192:358
Kwaansa-Ansah EE, Nti OS, Opoku F (2019) Heavy metals concentration and human health risk assessment in seven commercial fish species from Asafo Market, Ghana. Food Sci Biotechnol 28(2):569–579
Lanceleur L, Schäfer J, Chiffoleau J-F, Blanc G, Auger D, Renault S et al (2011) Long-term records of cadmium and silver contamination in sediments and oysters from the Gironde fluvial-estuarine continuum – evidence of changing silver sources. Chemosphere 85:1299–1305
Lortholarie M, Zalouk-Vergnoux A, Couderc M, Kamari A, François Y, Herrenknecht C, Poirier L (2020) Rare earth element bioaccumulation in the yellow and silver European eel (Anguilla anguilla): a case study in the Loire estuary (France). Sci Total Environ 719:134938. https://doi.org/10.1016/j.scitotenv.2019.134938
Liu Q, Liao Y, Shou L (2018) Concentration and potential health risk of heavy metals in seafoods collected from Sanmen Bay and its adjacent areas, China. Mar Pollut Bull 131:356–364
Maes GE, Raeymaekers JAM, Pampoulie C, Seynaeve A, Goemans G, Belpaire C et al (2005) The catadromous European eel Anguilla anguilla (L.) as a model for freshwater evolutionary ecotoxicology: relationship between heavy metal bioaccumulation, condition and genetic variability. Aquat Toxicol 73:99–114
Mata HK, Sivalingam P, Konde J, Otamonga J-P, Niane B, Mulaji CK et al (2020) Concentration of toxic metals and potential risk assessment in edible fishes from Congo River in urbanized area of Kinshasa, DR Congo. Hum Ecol Risk Assess Int J 26(6):1676–1692
Mendiburu F (2020) Agricola: statistical procedures for agricultural research. R package version 1.3–3. https://CRAN.R-project.org/package=agricolae
Miao X, Hao Y, Tang X, Xie Z, Liu L, Luo S et al (2020) Analysis and health risk assessment of toxic and essential elements of the wild fish caught by anglers in Liuzhou as a large industrial city of China. Chemosphere 243(2020):125337
Miri M, Akbari E, Amrane A, Jafari SJ, Eslami H, Hoseinzadeh E et al (2017) Health risk assessment of heavy metal intake due to fish consumption in the Sistan region, Iran. Environ Monit Assess 189:1–10
Öğlü B, Bhele U, Järvalt A, Tuvikene L, Timm H, Seller S et al (2020) Is fish biomass controlled by abiotic or biotic factors? Results of long-term monitoring in a large eutrophic lake. J Great Lakes Res 46(4):881–890
Özdemir N (1998) Environmental Issues and DALKO (Cooperative Fisheries Dalyan), the Socio-Economic Structure of Köyceğiz Basin, Ph.D. Thesis, Department of Fisheries, Institute of Science, Ege University
Pannetier P, Caron A, Campbell P-GC, Pierron F, Baudrimont M, Couture P (2016) A comparison of metal concentrations in the tissues of yellow American eel (Anguilla rostrata) and European eel (Anguilla anguilla). Sci Total Environ 569–570:1435–1445
Pierron F, Baudrimont M, Dufour S, Elie P, Bossy A, Baloche S et al (2008) How cadmium could compromise the completion of the European eel’s reproductive migration. Environ Sci Technol 42:4607–4612
Polak-Juszczak L, Robak S (2015) Macro- and microelements in eel (Anguilla anguilla) from the northern regions of Poland. J Elem 20(2):385–394. https://doi.org/10.5601/jelem.2014.19.2.652
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistics. Computing, Vienna, Austria. URL R: The R Project for Statistical Computing
Sankar TV, Zynudheen AA, Anandan R, Nair PGV (2006) Distribution of organochlorine pesticides and heavy metal residues in fish and shellfish from Calicut region, Kerala, India. Chemosphere 65:583–590
Sekhar KC, Chary NS, Kamala CT (2004) Fractionation studies and bioaccumulation of sediment-bound heavy metals in Kolleru Lake by edible fish. Environ Int 29:1001–1008
Sen I, Shandil A, Shrivastava VS (2011) Study for determination of heavy metals in fish species of the River Yamuna (Delhi) by Inductively Coupled Plasma Optical -Emission Spectroscopy (ICP-OES). Adv Appl Sci Res 2:161–166. Available online at https://www.pelagiaresearchlibrary.com
Sivaperumal P, Sankar TV, Viswanathan Nair PG (2007) Heavy metal concentrations in fish, shellfish and fish products from internal markets of India vis-a-vis international standards. Food Chem 102:612–620
Topcuoglu S, Kırbas Oglu C, Gungor N (2002) Heavy metals in organisms and sediments from the Turkish Coast of the Black Sea, 1997–1998. Environ Int 27:521–526
Traina A, Bono G, Bonsignore M, Falco F, Giuga M, Quinci EM et al (2019) Heavy metals concentrations in some commercially key species from Sicilian coasts (Mediterranean Sea): potential human health risk estimation. Ecotoxicol Environ Saf 168:466–478
Ubl C, Dorow M (2015) A novel enclosure approach to assessing yellow eel (Anguilla anguilla) density in non-tidal coastal waters. Fish Res 161:57–63
Usero J, Izquierdo C, Morillo J, Gracia I (2003) Heavy metals in fish (Solea vulgaris, Anguilla anguilla and Liza aurata) from salt marshes on the southern Atlantic coast of Spain. Environ Int 29(7):949–956
Zakir HM, Eti MSA, Quadir QF, Mallick S (2019) Health risk assessment of heavy metal intake of common fishes available in the Brahmaputra River of Bangladesh. Arch Curr Res Int 19(2):1–15
Zerizghi T, Yang Y, Wang W, Zhou YJ, Zhang J, Yi Y (2020) Ecological risk assessment of heavy metal concentrations in sediment and fish of a shallow lake: a case study of Baiyangdian Lake North China. Environ Monit Assess 192:154
Zhu F, Qu L, Fan W, Wang A, Hao H, Li X et al (2015) Study on heavy metal levels and its health risk assessment in some edible fishes from Nansi Lake, China. Environ Monit Assess 187:161
Funding
This research was funded by Muğla Sıtkı Koçman University Department of Scientific Research Projects Coordination with project number BAP 17/147 and Estonian Environmental Investment Centre project T180209PKKH, Estonia-Russia Cross Border Cooperation Programme 2014–2020 project ER80 “Restocking of European eel as a measure of recovery of endangered species and preservation of natural diversity,” Estonian University of Life Sciences research and development fond project nr PM170155PKLJ, and Estonian Research Council Grant PRG709.
Author information
Authors and Affiliations
Contributions
Ahmer Demirak: conceptualization, writing original draft, reviewing, and editing.
Feyyaz Keskin: eel samples collection (in Turkey and Estonia), digestion and analysis, literature researach, and writing.
Maidu Silm: preparation, literature research editing.
Deniz Yıldız: samples digestion and analysis, writing.
Nedim Özdemir: eel samples collection (in Turkey) and preparation, literature research.
Priit Bernotas: sample collection (in Estonia), preparation, editing.
Burak Öğlü: statistical analysis, sample collection, preparation, writing, editing.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable (this paper does not contain studies involving human participants, or their tissues.).
Consent for publication
Not applicable (this scientific paper does not contain any individual person’s or institution’s data in any form).
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Philippe Garrigues
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Demirak, A., Keskin, F., Silm, M. et al. Bioaccumulation and health risk assessment of heavy metals in European eels taken from Lakes Köyceğiz (Turkey) and Võrtsjärv (Estonia). Environ Sci Pollut Res 29, 1620–1633 (2022). https://doi.org/10.1007/s11356-021-16822-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-16822-x