Abstract
In this study, the eggs of 30 wild Black Sea whiting (Merlangius merlangus euxinus, Nordmann, 1840) and 30 farmed freshwater rainbow trout (Oncorhynchus mykiss, Walbaum, 1792) collected from Samsun Province in Turkey were analyzed to determine the level of contamination by nine organochlorine pesticides (OCPs), namely α-hexachlorocyclohexane (α-HCH), β-HCH, γ-HCH (lindane), hexachlorobenzene (HCB), aldrin, 2,4′-dichlorodiphenyltrichloroethane (DDT), 4,4′-DDT, 2,4′-dichlorodiphenyldichloroethylene (DDE), 4,4′-DDE, and 15 polychlorinated biphenyls (PCBs) (PCB-28, -70, -74, -81, -99, -101, -118, -138, -153, -156, -170, -180, -183, -187, and -208), and their potential use as biomarkers to monitor levels of environmental contamination. OCPs and PCBs in the fat of fish eggs were extracted cryogenically and their concentrations were determined with a gas chromatography-electron capture detector (GC-ECD). The whiting eggs showed high OCP and PCB levels compared to the rainbow trout eggs. The median ∑ DDT values for whiting and rainbow trout eggs were 1601.62 ng g−1 fat (range 824.87–5049.81) and 406.49 ng g−1 fat (range 199.88–588.82); median ∑Indicator PCBs were 1264.24 ng g−1 fat (range 520.05–6140.32) and 82.11 ng g−1 fat (range 2.85–215.97); and median ∑ HCHs were 155.66 ng g−1 fat (range 35.45–330.40) and 13.48 ng g−1 fat (range 4.44–66.44), respectively. In the whiting eggs, the ∑Indicator PCB level was above the maximum residue limit (MRL) of 200 ng g−1 fat stated in the European Commission Regulation (EC) and Turkish Food Codex (TFC). In addition, there was a significant difference between the contamination levels of the eggs of the two species. In conclusion, it appears that fish eggs can serve as a valuable biomarker for the level of contamination of persistent organochlorine contaminants in different aquatic environments.
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References
Aksoy A, Das YK, Yavuz O, Guvenc D, Atmaca E, Agaoglu S (2011) Organochlorine pesticide and polychlorinated biphenyls levels in fish and mussel in Van region, Turkey. Bull Environ Contam Toxicol 87:65–69. https://doi.org/10.1007/s00128-011-0286-z
Aksoy A, Guvenc D, Yavuz O, Das YK, Atmaca E (2012) Seasonal variation of polychlorinated biphenyls and organochlorine pesticide levels of sea and cultured farm fish in the Samsun region of Turkey. Bull Environ Contam Toxicol 88:842–849. https://doi.org/10.1007/s00128-012-0561-7
Ankley GT, Tillitt DE, Giesy JP, Jones PD, Verbrugge DA (1991) Bioassay-derived 2,3,7,8-tetrachlorodibenzo-para-dioxin equivalents in PCB-containing extracts from the flesh and eggs of Lake-Michigan chinook salmon (Oncorhynchus tshawytscha) and possible implications for reproduction. Can J Fish Aquat Sci 48:1685–1690. https://doi.org/10.1139/f91-200
Ben Ameur W, el Megdiche Y, Eljarrat E, Ben Hassine S, Badreddine B, Souad T, Bèchir H, Barceló D, Ridha Driss M (2013) Organochlorine and organobromine compounds in a benthic fish (Solea solea) from Bizerte Lagoon (northern Tunisia): implications for human exposure. Ecotoxicol Environ Saf 88:55–64. https://doi.org/10.1016/j.ecoenv.2012.10.021
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/o59-099
Bordet F, Inthavong D, Fremy J-M (2002) Interlaboratory study of a multiresidue gas chromatographic method for determination of organochlorine and pyrethroid pesticides and polychlorobiphenyls in milk, fish, eggs, and beef fat. J AOAC Int 85:1398–1409
Cakirogullari GC, Secer S (2011) Seasonal variation of organochlorine contaminants in bonito (Sarda sarda L. 1758) and anchovy (Engraulis encrasicolus L. 1758) in Black Sea region, Turkey. Chemosphere 85:1713–1718. https://doi.org/10.1016/j.chemosphere.2011.09.017
Coatu V, Oros A, Tiganus D, Lazar L (2015) Assessment of chemical contamination in biota from Romanian marine waters in respect with maximum admissible levels regulated by legislation for human consumption. J Environ Prot Ecol 16:117–125
EC (2006) European Commission, setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union. https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2006:364:0005:0024:EN:PDF. Accessed 17 September 2018
Fang W et al (2007) Organochlorine pesticides in soils under different land usage in the Taihu Lake region, China. J Environ Sci 19:584–590. https://doi.org/10.1016/S1001-0742(07)60097-7
Ferrante MC, Fusco G, Naccari C, Meli R, Clausi MT (2016) Are biometric parameters helpful to assess the health risk of consuming organochlorine compounds contaminated silver European eel (Anguilla anguilla)? J Food Sci 81:T1024–T1030. https://doi.org/10.1111/1750-3841.13259
Galaţchi M, Oros A, Coatu V, Costache M, Coprean D, Galaţchi L-D (2017) Pollutant bioaccumulation in anchovy (Engraulis encrasicolus) tissue, fish species of commercial interest at the Romanian Black Sea coast. OUAC 28:11–17. https://doi.org/10.1515/auoc-2017-0003
Hook SE, Gallagher EP, Batley GE (2014) The role of biomarkers in the assessment of aquatic ecosystem health. Integr Environ Assess Manag 10:327–341. https://doi.org/10.1002/ieam.1530
Hosseini SV, Behrooz RD, Esmaili-Sari A, Bahramifar N, Hosseini SM, Tahergorabi R, Hosseini SF, Feás X (2008) Contamination by organochlorine compounds in the edible tissue of four sturgeon species from the Caspian Sea (Iran). Chemosphere 73:972–979. https://doi.org/10.1016/j.chemosphere.2008.06.036
Jensen S, Häggberg L, Jörundsdóttir H, Odham G (2003) A quantitative lipid extraction method for residue analysis of fish involving nonhalogenated solvents. J Agric Food Chem 51:5607–5611. https://doi.org/10.1021/jf0301201
Lyons K, Lowe CG (2013) Quantification of maternal offloading of organic contaminants in elasmobranchs using the histotrophic round stingray (Urobatis halleri) as a model. Environ Sci Technol 47:12450–12458. https://doi.org/10.1021/es402347d
Madenjian CP, Ebener MP, Sepúlveda MS (2015) PCB concentrations of lake whitefish (Coregonus clupeaformis) vary by sex. J Great Lakes Res 41:1185–1190. https://doi.org/10.1016/j.jglr.2015.09.010
Malakhova L, Voronov V (2008) Organochlorine pollution of mariculture objects of the Crimea coastal area (Black Sea). In: Faye B, Sinyavskiy Y (eds) Impact of pollution on animal products. NATO science for peace and security series C-environmental security. Springer, Dordrecht, pp 169–176. https://doi.org/10.1007/978-1-4020-8359-4_18
Miller M, Amrhein J (1995) Maternal transfer of organochlorine compounds in Lake Superior siscowet (Salvelinus namaycush siscowet) to their eggs. Bull Environ Contam Toxicol 55:96–103. https://doi.org/10.1007/BF00212394
Miller MA (1993) Maternal transfer of organochlorine compounds in salmonines to their eggs. Can J Fish Aquat Sci 50:1405–1413. https://doi.org/10.1139/f93-161
Ondarza PM, Gonzalez M, Fillmann G, Miglioranza KSB (2014) PBDEs, PCBs and organochlorine pesticides distribution in edible fish from Negro River basin, Argentinean Patagonia. Chemosphere 94:135–142. https://doi.org/10.1016/j.chemosphere.2013.09.064
Peakall DB, Walker CH (1994) The role of biomarkers in environmental assessment (3). Vertebrates. Ecotoxicology 3:173–179. https://doi.org/10.1007/bf00117082
Samsun S, Erdem Y, Kalayci F (2011) Feeding regime of whiting (Gadus merlangus euxinus Nordmann, 1840) in Turkish middle Black Sea coast. Turk J Fish Aquat Sci 11:515–522. https://doi.org/10.4194/1303-2712-v11_4_02
Ssebugere P, Kiremire BT, Kishimba M, Wandiga SO, Nyanzi SA, Wasswa J (2009) DDT and metabolites in fish from Lake Edward, Uganda. Chemosphere 76:212–215. https://doi.org/10.1016/j.chemosphere.2009.03.049
Stancheva M, Georgieva S, Makedonski L (2017) Polychlorinated biphenyls in fish from Black Sea, Bulgaria. Food Control 72:205–210. https://doi.org/10.1016/j.foodcont.2016.05.012
Stoichev T, Makedonski L, Trifonova T, Stancheva M, Ribarova F (2007) DDT in fish from the Bulgarian region of the Black Sea. Chem Ecol 23:191–200. https://doi.org/10.1080/02757540701339851
Sudaryanto A, Monirith I, Kajiwara N, Takahashi S, Hartono P, Muawanah, Omori K, Takeoka H, Tanabe S (2007) Levels and distribution of organochlorines in fish from Indonesia. Environ Int 33:750–758. https://doi.org/10.1016/j.envint.2007.02.009
TFC (2011) Turkish Food Codex, Turk Gida Kodeksi Bulasanlar Yonetmeligi. Resmi Gazete. http://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-8.htm. Accessed 17 September 2018
Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149. https://doi.org/10.1016/S1382-6689(02)00126-6
Wilson P, Tillitt D (1996) Rainbow trout embryotoxicity of a complex contaminant mixture extracted from Lake Michigan lake trout. Mar Environ Res 42:129–134. https://doi.org/10.1016/0141-1136(95)00047-X
Zhang X, Gandhi N, Bhavsar SP (2016) Persistent organohalogens in paired fish fillet and eggs: implications for fish consumption advisories. J Agric Food Chem 64:2832–2840. https://doi.org/10.1021/acs.jafc.6b00089
Zhou R, Zhu L, Chen Y, Kong Q (2008) Concentrations and characteristics of organochlorine pesticides in aquatic biota from Qiantang River in China. Environ Pollut 151:190–199. https://doi.org/10.1016/j.envpol.2007.02.015
Zhulidov AV et al (2003) A review of riverine fluxes of hexachlorocyclohexane and DDT to the Azov and black seas from the former USSR and Russian federation. J Environ Sci Health A Tox Hazard Subst Environ Eng 38:753–769. https://doi.org/10.1081/ese-120018589
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Atmaca, E., Das, Y.K., Yavuz, O. et al. An evaluation of the levels of organochlorine compounds (OCPs and PCBs) in cultured freshwater and wild sea fish eggs as an exposure biomarker for environmental contamination. Environ Sci Pollut Res 26, 7005–7012 (2019). https://doi.org/10.1007/s11356-019-04207-0
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DOI: https://doi.org/10.1007/s11356-019-04207-0