Uluabat Gölü Su Kirliliğine Bağlı Olarak Cyprinus carpio ve Silurus glanis’teki Genetik Hasar Düzeyinin Belirlenmesi

Öz

Yeryüzünde gerek insan gerekse suda yaşayan organizmaların yaşamlarının devamlılığı açısından temiz su kaynakları giderek azalmaktadır. Tarımsal faaliyetler, sanayi atıkları ve evsel atıklardan kaynaklı gibi birçok kirletici suların kirlenmesine neden olmaktadır. Farklı kaynaklardan sulara karışan toksikantlar nedeniyle sularda yaşayan organizmalarda çeşitli genetik hasarlar ortaya çıkabilmektedir. Genetik materyaldeki hasarlar, sucul organizmaların adaptasyon kapasitesinde düşüş ve avcıdan kaçış gibi davranışlarda yetersizlik gibi yaşamsal önemde sorun yaratabilmektedir. Bu nedenle, organizmanın hayatta kalabilme yeterliliğinin korunabilmesi için genetik materyalin stabilitesi önemlidir. Bu çalışmada Uluabat Gölü’ndeki genotoksik potansiyel, farklı lokaliteden toplanan Cyprinus carpio (Sazan balığı) ve Silurus glanis (Yayın balığı) üzerinde tek hücre alkali jel elektroforezi (KOMET) ve mikronukleus (MN) teknikleri ile değerlendirilmiştir. Elde edilen sonuçlara göre Uluabat Gölü’nde ilkbahar ve yaz mevsimlerinde alınan kan örneklerindeki genotoksisite potansiyeli kış mevsimine göre yüksek bulunmuştur. Ayrıca su ve sedimente ait 9 farklı ağır metalin (Pb, Cd, Hg, As, Ni, Cr, Cu, Zn ve Mn) birikim düzeyleri analiz edilmiştir. Balık dokularında yapılan analiz sonuçlarına göre Hg kasta, As ve Zn böbrekte, Pb, Cd, Ni, Cr, Cu ve Mn karaciğerde daha fazla birikim gözlenmiştir.

Anahtar Kelimeler

• Uluabat Gölü
• Cyprinus carpio
• Silurus glanis
• Genotoksisite
• Ağır metal

Determination of Genetic Damage Level in Cyprinus carpio and Silurus glanis Depending on Uluabat Lake Water Pollution

Öz

The clean water resources necessary for human and aquatic organisms for the continuity of their lives are gradually decreasing. Agricultural activities, industrial wastes and domestic wastes cause pollution in waters. Genetic damages can occur in aquatic organisms due to toxicants that enter the water from different sources. Damage to genetic material can cause vital problems such as a decrease in the adaptation capacity of aquatic organisms, and inability to escape from predators. Therefore, the stability of the genetic material is important in order to maintain the survival of the organism. In this study, the genotoxic potential in Lake Uluabat was evaluated bythe alkaline single cell gel electrophoresis (COMET) and micronucleus (MN) techniques on Cyprinus carpio (common carp) and Silurus glanis (European catfish) collected from five different locality. According to the results, the genotoxicity potential in the blood samples taken was found to be higher in the spring and summer seasons than in the winter season of the lake. In addition, the accumulation levels of 9 different heavy metals (Pb, Cd, Hg, As, Ni, Cr, Cu, Zn and Mn) in water and sediment were analyzed. It was determined that in the samples taken from fish tissues, the highest Hg accumulation was found in muscle, As and Zn in kidney, Pb, Cd, Ni, Cr, Cu and Mn in liver.

Anahtar Kelimeler

• Lake Uluabat
• Cyprinus carpio
• Silurus glanis
• genotoxicity
• heavy metal

Kaynakça

1. Ahuja S. 2013. Monitoring water quality: Pollution assessment, analysis, and remediation. Oxford: Elsevier 379 p.
2. Aksoy E, Özsoy G. 2002. Investigation of multi-temporal land use/cover and shoreline changes of the Uluabat Lake Ramsar Site using RS and GIS. Paper presented at: International Conference on Sustainable Land Use and Management; Çanakkale, Turkey. Proceedings Book. 318-325.
3. Al-Sabti K, Metcalfe CD. 1995. Fish micronuclei for assessing genotoxicity in water. Mutat Res-Genet Tox. 343(2-3):121–135. doi: 10.1016/0165-1218(95)90078-0
4. Anonim 2004. Türkiye Çevre Atlası. T.C. Çevre ve Orman Bakanlığı ÇED ve Planlama Genel Müdürlüğü, Ankara; [Erişim tarihi: 01.10.2020]. Erişim Adresi:https://webdosya.csb.gov.tr/db/ced/ icerikler/turk-yecevreatlas--20180514084340.pdf
5. Anonim 2016. Uluabat Gölü alt havzası su kalitesi eylem planı. Ankara: Orman ve Su İşleri Bakanlığı Su Yönetimi Genel Müdürlüğü Su Kalitesi Yönetimi Dairesi Başkanlığı 38 s.
6. APHA. 1993. Standard methods for the examination of water and wastewater. Washington StatSoft Inc. 1993. CSS (Complete Statistica System): Statistica, References for statistical procedures DOS and Windows version), Release 3.1. StatSoft Inc., Tulsa, OK.
7. Arslan OC, Parlak, H, Katalay S, Boyacıoğlu M, Karaaslan MA, Güner H. 2010. Detecting micronuclei frequency in some aquatic organisms for monitoring pollution of Izmir Bay (Western Turkey). Environ Monit Assess. 165(1-4):55-66. doi: 10.1007/s10661-009-0926-5
8. ASTM 1985. Preparation of biological samples for inorganic chemical analysis 1, Annual Book of ASTM Standards, D-19.

9. Ateeq B, Abul Farah M, Ahmad W. 2005. Detection of DNA damage by alkaline single cell gel electrophoresis in 2,4-dichlorophenoxyacetic-acid- and butachlorexposed erythrocytes of Clarias batrachus. Ecotox Environ Safe. 62(3):348–354. doi: 10.1016/j.ecoenv.2004.12.011
10. Barlas N, Aköz N, Aydoğan M. 2005. Assessment of heavy metal residues in the sediment and water samples of Uluabat Lake, Turkey. B Environ Contam Tox. 74(2):286-293. doi: 10.1007/s00128-004-0582-y
11. Barlas N, Çok İ, Akbulut N. 2006. The contamination levels of organochlorine pesticides in water and sediment samples in Uluabat Lake, Turkey. Environ Monit Assess. 118(1-3):383–391. doi: 10.1007/s10661-006-1504-8
12. Barsiene J, Rybakovas A, Lang T, Grygiel W, Andreikenaite L, Michailovas A. 2012. Risk of environmental genotoxicity in the Baltic Sea over the period of 2009-201 assessed by micronuclei frequencies in blood erythrocytes of flounder (Platichthys flesus), herring (Clupea harengus) and eelpout (Zoarces viviparus). Marine Environ Res. 77:35-42. doi: 10.1016/j.marenvres.2012.01.004
13. Bianchi E, Goldoni A, Trintinaglia L, Lessing G, Silva CEM, Nascimento CA, Ziulkoski AL, Spilki FR, Silva LB. 2013. Evaluation of genotoxicity and cytotoxicity of water samples from the Sinos River Basin, southern Brazil. Braz J Biol. 75(2):68-74. doi: 10.1590/1519-6984.1913
14. Blume KK, Macedo JC, Meneguzzi A, Silva LB, Quevedo DM, Rodrigues MAS. 2010. Water quality assessment of the Sinos River, Southern Brazil. Braz J Biol. 70(4):1185-1193. doi: 10.1590/1519-6984.01613suppl
15. Bulut C, Atay R, Uysal K, Köse E, Çınar S, 2010. Uluabat Gölü yüzey suyu kalitesinin değerlendirilmesi. Istanbul University Journal of Fisheries Aquatic Sciences. 25(1):9-18.
16. Buschini A, Carboni P, Martino A, Poli P, Rossi C. 2003. Effects of temperature on baseline and genotoxicant-induced DNA damage in haemocytes of Dreissena polymorpha, Mutat Res-Gen Tox En. 537(1):81-92. doi: 10.1016/S1383-5718(03)00050-0
17. Chen G, Paul A, White PA. 2004. The mutagenic hazards of aquatic sediments: a review. Mutat Res-Rev Mutat. 567(2-3):151-225. doi: 10.1016/j.mrrev.2004.08.005
18. Cok I, Ulutas OK, Okusluk O, Durmaz E, Demir N. 2011. Evaluation of DNA damage in common carp (Cyprinus carpio L.) by comet assay for determination of possible pollution in Lake Mogan (Ankara). The Scientific World Journal. 11:1455-1461. doi: 10.1100/tsw.2011.140
19. Collins AR. 2005. Assays for oxidative stres and antioxidant status: Applications to research into the biological effectiveness of polyphenols. Am J Clin Nutr. 81(1):261S-267S. doi: 10.1093/ajcn/81.1.261S
20. Çalıseki M, Işık G, Leblebici S. 2016. Porsuk Nehri suyunun Cucumis Sativus (L.) tohumlarının fide gelişimi üzerine etkilerinin belirlenmesi. Anadolu Üniversitesi Bilim ve Teknoloji Dergisi C- Yaşam Bilimleri ve Biyoteknoloji. 4(2):77-80.
21. Çiçek A, Arslan N, Koç B, Malkoç S, Emiroğlu Ö. 2008. Determination of lead levels in lake water, sediment, meiobenthos (Chironomidae) and three fish species from Lake Uluabat (A Ramsar Site in Turkey). The 12th World Lake Conference (Taal 2007); Rajasthan, Hindistan.
22. Dalkıran N, Zünbülgil B, Karacaoğlu D, Dere Ş. 2016. Uluabat Gölü epifitik diyatomelerinin uzun dönemdeki değişimi. LimnoFish 2(3):153-163. doi: 10.17216/limnofish.279724
23. De Andrade VM, Da Silva J, Da Silva FR, Heuser VD, Dias JF. Yoneama ML, De Freitas TRO. 2004. Fish as bioindicators to assess the effects of pollution in two southern Brazilian rivers using the comet assay and micronucleus test. Environ Mol Mutagen. 44(5):459-468. doi: 10.1002/em.20070
24. Demir E, Kaya B. 2013. Studies on the genotoxic properties of four benzyl derivatives in the In vivo comet assay using haemocytes of Drosophila melanogaster. Fresen Environ Bull. 22(5):1590-1596.
25. Demir E, Kaya N, Kaya B. 2011. Evaluation of DNA damage in Capsicum annuum L. exposed to spinosad in the comet assay. Fresen Environ Bull. 20(8):1926-1930.
26. Demir E, Kaya N, Kaya B. 2014. Genotoxic effects of zinc oxide and titanium dioxide nanoparticles on root meristem cells of Allium cepa by comet assay. Turk J Biol. 38(1):31-39. doi: 10.3906/biy-1306-11
27. Demir E, Kocaoğlu S, Kaya B. 2010. Assessment of genotoxic effects of benzyl derivatives by the comet assay. Food Chem Toxicol. 48(5):1239-1242. doi: 10.1016/j.fct.2010.02.016
28. Deng J, Wang Y, Liu X, Hu W, Zhu J, Zhu L. 2016. Spatial distribution and risk assessment of heavy metals and As pollution in the sediments of a shallow lake. Environ Monit Assess. 188(5):296. doi: 10.1007/s10661-016-5301-8
29. Deutschmann B, Kolarevic S, Brackc W, Kaisarevic S, Kostic J, Kracun-Kolarevic M, Liska I, Paunovic M, Seiler T-B, Shao Y, Sipos S, Slobodnik J, Teodorovic I, Vukovic-Gacic B, Hollert H. 2016. Longitudinal profile of the genotoxic potential of the River Danube on erythrocytes of wild common bleak (Alburnus alburnus) assessed using the comet and micronucleus assay. Sci Total Environ. 573:1441-1449. doi: 10.1016/j.scitotenv.2016.07.175
30. Elmacı A, Teksoy A, Topaç FO, Özengin N, Başkaya HS. 2008. Uluabat Gölünün mikrobiyolojik özelliklerinin mevsimsel değişiminin izlenmesi. Uludağ Üniversitesi Mühendislik-Mimarlık Fakültesi Dergisi. 13(1):93-103. doi: 10.17482/uujfe.93575
31. Elmacı A, Topaç OTi Teksoy A, Özengin N, Başkaya HS. 2010. Uluabat Gölü fizikokimyasal özelliklerinin yönetmelikler çerçevesinde değerlendirilmesi. Uludağ Üniversitesi Mühendislik-Mimarlık Fakültesi Dergisi, 15(1):149-157. doi: 10.17482/uujfe.34872
32. EPA 1994 (Environmental Protection Agency) Method 200.7. 1994. Determination of metals and trace elements in water and wastes by inductively coupled plasma-atomic emission spectrometry; [Erişim tarihi: 04.11.2020]. Erişim Adresi: https://www.epa.gov/sites/production/files/2015-06/documents/epa-200.7.pdf
33. EPA 1998 (Environmental Protection Agency) Method 3051, 1998. Microwave assisted acid digestion of sediments, sludges, soils, and oils. [Erişim tarihi: 04.11.2020]. Erişim Adresi: https://www.epa.gov/sites/production/files/2015-12/documents/3051a.pdf
34. Galindo TP, Moreira L. 2009. Evaluation of genotoxicity using the micronucleus assay and nuclear abnormalities in the tropical sea fish Bathygobius soporator (Valenciennes, 1837) (Teleostei, Gobiidae). Genet Mol Biol. 32(2):394-398. doi: 10.1590/S1415-47572009000200029
35. Goldberg DE. 1976. The health of oceans. Paris: The Unesco press 172 p.
36. Grisolia CK, Rivero CLG, Starling FLRM, Silva ICR, Barbosa AC, Dorea JG. 2009. Profile of micronucleus frequencies and DNA damage in different species of fish in a eutrophic tropical lake. Genet Mol Biol. 32(1):138-143. doi: 10.1590/S1415-47572009005000009
37. Gümüş NE, Akköz C. 2020. Eber Gölü (Afyonkarahisar) su kalitesinin araştırılması. LimnoFish. 6(2):153-163. doi: 10.17216/limnofish.638567
38. Has-Schön E, Bogut I, Vukovic R, Galovic D, Bogut A, Horvatic J. 2015. Distribution and age-related bioaccumulation of lead (Pb), mercury (Hg), cadmium (Cd), and arsenic (As) in tissues of common carp (Cyprinus carpio) and European catfish (Silurus glanis) from the Buško Blato reservoir (Bosnia and Herzegovina). Chemosphere. 135:289-296. doi: 10.1016/j.chemosphere.2015.04.015
39. Hayashi M, Ueda T, Uyeno K, Wada K, Kınae N, Saotome K, Tanaka N, Takaı A, Sasakı YF, Asano N, Sofunı T, Ojıma Y. 1998. Development of genotoxicity assay systems that use aquatic organisms. Mutat Res-Fund Mol M. 399(2):125-133. doi: 10.1016/s0027-5107(97)00251-0
40. Huuskonen S, Räsänen T, Koponen K, Lindström-Seppä P. 1995. Time-course studies of the biotrasformation enzymes in control rainbow trout when adjusting to new habitats. Marine Environ Res. 39(1-4):79-83. doi: 10.1016/0141-1136(94)00043-O
41. Hu C, Deng Z, Xie Y, Chen X, Feng LF. 2015. The risk assessment of sediment heavy metal Pollution in the East Dongting Lake Wetland. J Chem NY. Article ID 835487. doi: 10.1155/2015/835487
42. Kaoud HA, El-Dahshan AR. 2010. Bioaccumulation and histopathological alterations of the heavy metals in Oreochromis niloticus fish. Nature and Science. 8(4):147-156.
43. Klobucar GIV, Malev O, Srut M, Stambuk A, Lorenzon S, Cvetkovıc Z, Ferrero EA, Maguıre I. 2012. Genotoxicity monitoring of freshwater environments using caged crayfish (Astacus leptodactylus). Chemosphere. 87(1):62-67. doi: 10.1016/j.chemosphere.2011.11.060
44. Klobucar GIV, Stambuk A, Pavlica M, Peric MS, Hackenberger BK, Hylland A. 2010. Genotoxicity monitoring of freshwater environments using caged carp (Cyprinus carpio). Ecotoxicology. 19(1):77–84 doi: 10.1007/s10646-009-0390-6
45. Kontaş S, Bostancı D. 2020. Balıklarda genotoksik hasarın belirlenmesine yönelik bir araştırma: Capoeta banarescui örneği. LimnoFish. 6(2):144-152 doi: 10.17216/limnofish.688645
46. Kosmehl T, Hallare AV, Braunbeck T, Hollert H. 2008. DNA damage induced by genotoxicants in zebrafish (Danio rerio) embryos after contact exposure to freeze-dried sediment and sediment extracts from Laguna Lake (The Philippines) as measured by the comet assay. Mutat Res-Gen Tox En. 650(1):1-14. doi: 10.1016/j.mrgentox.2007.09.009
47. Linde-Arias R.A, Inácio FA, Alburquerque C, Freire MM, Moreira CJ. 2008. Biomarkers in an invasive fish species, Oreochromis niloticus, to assess the effects of pollution in a highly degraded Brazilian River. Sci Total Environ. 399(1-3):186-192. doi: 10.1016/j.scitotenv.2008.03.028
48. Minareci O, Sungur Ö. 2019. Akgöl ve Gebekirse göllerinde (Selçuk, İzmir, Türkiye) bazı fiziko-kimyasal parametrelerin mevsimsel değişimi. Gümüşhane Üniversitesi Fen Bilimleri Enstitüsü Dergisi. 9(4):751-758. doi: 10.17714/gumusfenbil.528798
49. Mitchelmore C, Chipman J. 1998. Detection of DNA strand breaks in brown trout (Salmo trutta) hepatocytes and blood cells using the single cell gel electrophoresis (comet) assay. Aquat Toxicol. 41(1-2):161-182. doi: 10.1016/S0166-445X(97)00064-7
50. Nunes EA, De Lemos CT, Gavronskı L, Moreıra TN, Olıveıra NCD, Da Silva J. 2011. Genotoxic assessment on river water using different biological systems. Chemosphere. 84(1):47-53. doi: 10.1016/j.chemosphere.2011.02.085
51. Ohe T, Watanabe T, Wakabayashi K. 2004. Mutagens in surface waters: a review. Mutat Res-Rev Mutat. 567(2-3):109-149. doi: 10.1016/j.mrrev.2004.08.003
52. Omar WA, Zaghloulb KH, Abdel-Khaleka AA, Abo-Hegaba S. 2012. Genotoxic effects of metal pollution in two fish species, Oreochromis niloticus and Mugil cephalus, from highly degraded aquatic habitats. Mutat Res-Gen Tox En. 746(1):7-12. doi: 10.1016/j.mrgentox.2012.01.013
53. Osman AGM, Abuel-Fadl KY, Kloas W. 2012. In situ evaluation of the genotoxic potential of the river Nile: II. Detection of DNA strand-breakage and apoptosis in Oreochromis niloticus niloticus (Linnaeus, 1758) and Clarias gariepinus (Burchell, 1822). Mutat Res-Gen Tox En. 747(1):14-21. doi: 10.1016/j.mrgentox.2012.02.013
54. Otter RR, Meıer J, Kubach KM, Lazorchak JM, Klaıne SJ. 2012. The effects of urbanization on Lepomis macrochirus using the comet assay. Ecotox Environ Safe. 84:299-303. doi: 10.1016/j.ecoenv.2012.07.025
55. Penders EJM, Spenkelink A, Hoogenboezem W, Rotteveel SGP, Maas JL, Alink GM. 2012. Genotoxic effects in the Eastern mudminnow (Umbra pygmaea) after prolonged exposure to River Rhinewater, as assessed by use of the in vivo SCE and Comet assays. Environ Mol Mutagen. 53(4):304-310. doi: 10.1002/em.21687
56. Rajaguru P, Suba S, Palanivel M, Kalaiselvi K. 2003. Genotoxicity of a polluted river system measured using the alkaline Comet assay on fish and earthworm tissues. Environ Mol Mutagen. 41(2):85-91. doi: 10.1002/em.10134
57. Russo C, Rocco L, Morescalchi MA, Stingo V. 2004. Assessment of environmental stress by the micronucleus test and the Comet assay on the genome of teleost populations from two natural environments. Ecotox Environ Safe. 57(2):168-174. doi: 10.1016/S0147-6513(03)00027-7
58. Saleh KH, Alshehrı MA. 2011. The intensity of pollutant genotoxicity in Lake Uluabat: Investigation of the peripheral erythrocytes of Cyprinus carpio. Afr J Biotechnol. 10(71):16045-16050. doi: 10.5897/AJB09.1841
59. Salihoğlu G, Karaer F. 2005. Uluabat gölü için ekolojik risk değerlendirmesi. İtüdergisi/e Su Kirlenmesi Kontrolü. 15(1-3):17-28.
60. Sanchez-Galan S, Linde AR, Ayllon F, Garcia-Vazquez E. 2001. Induction of micronuclei in eel (Anguilla anguilla L.) by heavy metals. Ecotox Environ Safe. 49(2):139–143. doi: 10.1006/eesa.2001.2048
61. Saydam Eker Ç, Özkan Ö. 2017. Ankara Çayı dere yatağı sedimanlarının zararlı element içeriği. Gümüşhane Üniversitesi Fen Bilimleri Enstitüsü Dergisi. 7(2):208-220.
62. Schmid W. 1976. The micronucleus test for cytogenetic analysis. In: Hollaender A, editor. Chemical mutagens: principles and methods for their detection. Vol. 4. New York: Plenum Press. p. 31–53.
63. Schwarzenbach RP, Egli T, Hofstetter TB, Gunten U, Wehrli B. 2010. Global water pollution and human health. Annu Rev Env Resour. 35:109-136. doi: 10.1146/annurev-environ-100809-125342
64. Singh NP, Mccoy MT, Tice RR, Schneider EL. 1988. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp Cell Res. 175(1):184-191. doi: 10.1016/0014-4827(88)90265-0
65. Squadrone S, Prearo M, Brizio P, Gavinelli S, Pellegrino M, Scanzio T, Guarise S, Benedetto A, Abete MC. 2013. Heavy metals distribution in muscle, liver, kidney and gill of European catfish (Silurus glanis) from Italian Rivers. Chemosphere. 90(2):358–365. doi: 10.1016/j.chemosphere.2012.07.028
66. Summak S, Aydemir NC, Vatan Ö, Yilmaz D, Zorlu T, Bilaloğlu T. 2010. Evaluation of genotoxicity from Nilufer Stream (Bursa/Turkey) water using piscine micronucleus test. Food Chem Toxicol. 48(8-9):2443-2447. doi: 10.1016/j.fct.2010.06.007
67. Tice RR, Rews PW, Singh NP. 1990. The single cell gel assay. A sensitive technique for evaluating intercellular differences in DNA damage and repair. In: Sutherland BM, Wordhead AD, editors. DNA damage and repair in human tissues. New York: Plenum. p. 291-302.
68. Tokatli C, Çiçek A, Emiroğlu Ö, Arslan N, Köse E, Dayioğlu H. 2014. Statistical approaches to evaluate the aquatic ecosystem qualities of a significant mining area: Emet stream basin (Turkey). Environ Earth Sci. 71(5):2185–2197. doi: 10.1007/s12665-013-2624-4
69. Tunca E, Atasagun S. 2012. Yeniçağa (Bolu) Gölü’ndeki kerevitlerin (Astacus leptodactylus) bazı dokularındaki ağır metal birikimi. KSU Doğa Bil Derg. 15(1):46-51.
70. TÜİK 2013. Nüfus Projeksiyonları 2013-2075; [Erişim Tarihi: 09.11.2016]. Erişim Adresi: http://www.tuik.gov.tr/PreIstatistikTablo.do?istab_id=1637
71. Ulutaş OK, Okusluk O, Demir N, Durmaz E, Cok I. 2008. Determination of possible pollution in Lake Mogan (Ankara) by Comet assay using common carp (Cyprinus carpio L.). Toxicol Lett. 180:S204-S205. doi: 10.1016/j.toxlet.2008.06.242
72. Uslu O, Türkman A. 1987. Su kirliliği ve kontrolü, İzmir: T.C. Başbakanlık Çevre Genel Müdürlüğü Yayınları 56 s.
73. Ünlü S, Alpar B, Öztürk K, Vardar D. 2010. Polycyclic aromatic hydrocarbons (PAHs) in the surficial sediments from Lake Iznik (Turkey): spatial distributions and sources. Bull Environ Contam Tox. 85(6):573-580. doi: 10.1007/s00128-010-0134-6
74. Vincent-Hubert F, Heas-Moisan K, Munschy C, Tronczynskib J. 2012. Mutagenicity and genotoxicity of suspended particulate matter in the Seine river estuary. Mutat Res-Gen Tox En. 741(1-2):7-12. doi: 10.1016/j.mrgentox.2011.09.019
75. Wang Y, Chen P, Cui R, Si W, Zhang Y, Ji E. 2010. Heavy metal concentrations in water sediment and tissues of two fish species (Triplohysa pappenheimi, Gobio hwanghensis) from the Lanzhou section of the Yellow River, China. Environ Monit Assess. 165(1-4):97-102. doi: 10.1007/s10661-009-0929-2
76. Yang Y, Zhengchao Z, Yanying B, Yimin C, Weiping C. 2016. Risk assessment of heavy metal pollution in sediments of the Fenghe River by the fuzzy synthetic evaluation model and multivariate statistical methods. Pedosphere. 26(3):326-334. doi: 10.1016/S1002-0160(15)60046-7