A biomonitoring study: Using the biomarkers in Cyprinus carpio for the evaluation of water pollution in Sapanca lake (Sakarya, Turkey)

Year 2021, Volume: 5 Issue: 1, 107 - 121, 31.03.2021

Güllü Kaymak , Figen Esin Kayhan , Nazan Deniz Yön Ertuğ

https://doi.org/10.31015/jaefs.2021.1.14

Cited By: 3

Abstract

This study aims to determine the toxic effects of heavy metal pollution on carp (Cyprinus carpio) in Sapanca Lake by biochemical and histological analyses. For this reason, fish and water samples were taken from the lake in 2015. Heavy metal (Cu, Fe, Zn, Pb, Cd) analyzes in the water column and tissues (muscle, liver, gill) were determined by ICP-OES. CAT, GSH and MDA levels, which are oxidative stress bioindicators in tissues, were measured by spectrophotometric methods. Histopathological findings in tissues were determined by Hematoxylin-Eosin staining. As a result, heavy metal concentrations in water were determined as Fe > Zn > Pb > Cu > Cd. The accumulation of Cu, Fe and Cd in the tissues of the fish were liver > gill > muscle, and the accumulation of Zn was gill > liver > muscle. CAT activity, MDA and GSH level of the tissues changed with the water temperature. General signs of destruction were observed in the gill tissues of the fish. Necrotic conditions in hepatocytes were observed. In conclusion, the presence of biochemical and histopathological findings in tissues suggests that the lake is not only affected by heavy metals but also by other pollutants.

Keywords

Heavy metals, Carp, Oxidative stress, Fresh water, Histopathology

Supporting Institution

Sakarya Üniversitesi

Project Number

2015-50-02-007

Thanks

We thanks to the TÜBİTAK-BİDEB 2211-C National Doctoral Scholarship Program for Priority Areas as it provides financial support during the doctoral thesis study. We also thanks to the Sakarya University Scientific Research Projects (BAP) Commission (Project No: 2015-50-02-007), which allows this study to be financially supported.

References

• Abdel-Baki A.S., Dkhil M.A., AlQuraishy S. (2011). Bioaccumulation of some heavy metals in tilapia fish relevant to their concentration in water and sediment of Wadi Hanifah, Saudi Arabia. African Journal of Biotechnology, 10(13), 2541-2547. Doi: https://doi.org/10.5897/AJB10.1772
• Aboul Ezz A.S., Abdel-Razek S.E. (1991). Heavy metal accumulation in the Tilapia nilotica L. and in the waters of Lake Manzalah. Egypt. J Applied Sci 6, 37-52.
• Adasu General Directorate (2003). Sapanca Gölü Çevre Koruma Projesine Esas Bilgiler, Adapazarı (Basics of Sapanca Lake Environmental Protection Project, Adapazarı). (in Turkish)
• Aebi H. (1974). Catalase In vitro. In: Methods of Enzymatic Analysis. Ed: Bergmeyer HU, 2nd ed, FL, 121-126.
• Ahmad V.L., Maria M., Oliveira M., Pacheco M., Santos A. (2006). Oxidative stress and genotoxic effects in gill and kidney of Anguilla anguilla L. exposed to chromium with or without pre-exposure to betanaphthoflavone, Mutat. Res. 608, 16-28. Doi: https://doi.org/10.1016/j.mrgentox.2006.04.020
• Al-Bairuty G.A. (2013). Histopathological effects of metal and metalic nanoparticles on the body systems of rainbow trout (Oncorhynchus mykiss). Doctoral Thesis, University of Plymouth.
• Altug G., Okgerman H. (2008). Levels of some toxic elements in the surface sediment and some biota from the Sapanca Lake, Turkey. Fresenius Environmental Bulletin, 17(1), 24-28. https://www.prt-parlar.de/download_feb_2008/1
• Altundag H., Yıldırım E., Altıntıg E. (2019). Determination of some heavy metals by ICP-OES in edible parts of fish from Sapanca Lake and streams. Journal of Chemical Metrology, 13(1). Doi: http://doi.org/10.25135/jcm.24.19.03.1219
• AnvariFar H., Amirkolaie A.K., Jalali A. M., Miandare H.K., Sayed A.H., İşisağ-Üçüncü S., Ouraji H., Ceci M., Romano N. (2018). Environmental pollution and toxic substances: Cellular apoptosis as a key parameter in a sensible model like fish. Aquatic toxicology, 204:144-159. Doi: http://doi.org/10.1016/j.aquatox.2018.09.010
• Authman M.M., Zaki M.S., Khallaf E.A., Abbas H.H. (2015). Use of fish as bio-indicator of the effects of heavy metals pollution. Journal of Aquaculture Research & Development, 6(4), 1-13. Doi: http://doi.org/10.4172/2155-9546.1000328
• Bakan G., Balkas T.I. (1999). Enrichment of metals in the surface sediments of Sapanca Lake. Water Environment Research, 71 (1):71-74. Doi: http://doi.org/10.2175/106143099X121463
• Beutler E. (1975). Glutathione in Red Cell Metabolism: A Manual of Biochemical Methods, 2nd ed., Grune and Stratton, NY, 112-114.
• Bradford M.M. (1976). A Rapid and Sensitive Method for the Quantitation of Microgram Quantitites of Protein Utilizing the Principle of Protein-dye Binding. Analytical Biochemistry, 72, 248-254. Doi: https://doi.org/10.1016/0003-2697(76)90527-3
• Brand D.G., Fink R., Bengeyfield W., Birtwell I.K., McAllister C.D. (2001). Salt water-acclimated pink salmon fry (Oncorhynchus gorbuscha) develop stressrelated visceral lesions after 10-day exposure to sublethal concentrations of the water-soluble fraction of north-slope crude oil. Toxicologic Pathology, 9(5):574- 584. Doi: https://doi.org/10.1080/019262301317226384
• Bury N.R., Walker P.A., Glover C.N. (2003). Nutritive metal uptake in teleost fish. The Journal of Experimental Biology, 206:11-23. Doi: https://doi.org/10.1242/jeb.00068
• Çakır Z., Barka A., Akyüz S. (2010). Coulomb stress interactions and the 1999 Marmara earthquakes. İTÜ Dergisi/d, 2(4):1-4. https://journals.tubitak.gov.tr/earth/abstract.htm?id=6021
• Canpolat O., Eroglu M., Dusukcan M. (2016). Transfer factor of some heavy metals in muscle of Cyprinus carpio. Fresenius Environ Bull, 25(11), 4988-4994. https://www.prt-parlar.de/download_feb_2016/11
• Chen G., White P.A. (2004). The mutagenic hazards of aquatic sediments. A Review. Reviews in Mutation Research, 567:151-225. Doi: https://doi.org/10.1016/j.mrrev.2004.08.005
• Cheung C.C.C., Zheng G.J., Li A.M.Y., Richardson B.J., Lam P.K.S. (2001). Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of Marine Mussels, Perna viridis. Aquatic Toxicology, 52:189-203. Doi: https://doi.org/10.1016/S0166-445X(00)00145-4
• Dostbil M. (2010). Determination of heavy metal concentrations in water and sediment of mogan lake; examination of effects on tissues of carp (Cyprinus carpio) and tench (Tinca tinca). Master’s Thesis, Gazi University. (in Turkish).
• Duman F., Sezen G., Nilhan Tug G. (2007). Seasonal changes of some heavy metal concentrations in Sapanca Lake water, Turkey. International Journal of Natural on Engineering Sciences, 1(3):25-28.
• Dündar M.Ş., Altundağ H., Boz V., Akaya K., Sayın M. (2003). A Comparative Analysis of Same Trace Elements in Rivers Flow Through Sapanca Lake Before and After 17 August 1999 Marmara Earthquake. Anadolu University Journal of Science and Technology, 4 (2):205-210 (in Turkish).
• Engin M.S., Uyanik A., Cay S., Kir I. (2016). Evaluation of trace metals in sediment, water, and fish (Mugil cephalus) of the central Black Sea coast of Turkey. Human and Ecological Risk Assessment: An International Journal, 22(1): 241-250. Doi: https://doi.org/10.1080/10807039.2015.1057685
• Fırat Ö., Kargın F. (2010). Effects of zinc and cadmium on erythrocyte antioxidant systems of a freshwater fish Oreochromis niloticus. J. Biochem. Molecular Toxicology, 4:145-149. Doi: https://doi.org/10.1002/jbt.20327
• Fonseca A.R., Fernandes L.S., Fontainhas-Fernandes A., Monteiro S.M., Pacheco F.A.L. (2017). The impact of freshwater metal concentrations on the severity of histopathological changes in fish gills: A statistical perspective. Science of the Total Environment, 599: 217-226. DOI: https://doi.org/10.1016/j.scitotenv.2017.04.196
• Furia R.R. (2004). Preliminary aspects of water soluble fraction of diesel oil effects on gill histology of Trachinotus sp. behavior, physiology and toxicology interactions in fish. International Congress on the Biology of Fish. Manaus, Brazil, August 1-5, pp. 343-349.
• Gülcü-Gür, B., Tekin-Özan, S. (2017). The investigation of heavy metal levels in water and sediment from Işıklı Lake (Turkey) in relation to seasons and physicochemical parameters. Journal of Aquaculture Engineering and Fisheries Research, 3(2):87-96. Doi: https://doi.org/10.3153/JAEFR17012
• Güngördü A., Belda E., Dürdane K. (2012). Evaluation of spatial and temporal changes in biomarker responses in the common carp (Cyprinus Carpio L.) for biomonitoring The Meriç Delta, Turkey. Environmental Toxicology and Pharmacology, 33:431–439. Doi: https://doi.org/10.1016/j.etap.2012.01.003
• Hadi A.A., Alwan S.F. (2012). Histopathological changes in gills, liver and kidney of fresh water fish, Tilapia zillii, Exposed to Aluminum. International Journal of Pharmacy & Life Sciences, 3(11): 2071-2081.
• Heath A.G. (1987). Water pollution and fish physiology. CRP Press Inc. 245 s. Florida.
• Hermenean A., Damache G., Albu P., Ardelean A., Ardelean G., Ardelean D.P., Horge M., Nagy T., Braun M., Zsuga M., Kéki S., Costache M., Dinischiotu A. (2015). Histopatological alterations and oxidative stress in liver and kidney of Leuciscus cephalus following exposure to heavy metals in the Tur River, North Western Romania. Ecotoxicology and environmental safety, 119:198-205. Doi: https://doi.org/10.1016/j.ecoenv.2015.05.029
• Hesni M.A., Savari A., Sohrab A.D., Mortazavi M.S. (2011). Gill histopathological changes in milkfish (Chanos chanos) exposed to acute toxicity of diesel oil. World Applied Sciences Journal, 14(10):1487-1492.
• Hinton D., Lauren D. (1990). Liver structural alterations accompanying chronic toxicity in fishes: Potential biomarkers of exposure, in: Biomakers of environmental contamination, McCarthy, J. and Shugart, L. (Eds.), Lewis Publishers, Boca Raton, Florida.
• Hinton D.E., Segner H., Au D.W.T., Kullman S.W., Hartman R.C. (2008). Liver toxicity. In: The toxicology of fishes, Di Giulio RT, Hinton DE (Eds), CRC Press Inc., Florida.
• Hinton D.E., Segner H., Braunbeck T. (2001). Toxic responses of the liver. In: Daniel, S., Benson, W.H. (Eds.), Target organ toxicity in marine and freshwater teleosts, vol. 1, London.
• Holt E. A., Miller S. W. (2011). Bioindicators: using organisms to measure environmental impacts. Nature Education Knowledge, 3(10), 8.
• İşisağ Üçüncü S., Önen Ö., Ergen G., Üreten M., Boz E., Seferoğlu K., Gökçe B. (2010). The Effects of Dioctyl Adipate (DOA) on the gill histology of Labidochromis caeruleus Fryer, 1956 (Cichlidae, Teleostei). Kafkas Üniversitesi Veterinerlik Fakültesi Dergisi, 16(2):343-346. (In Turkish). Doi: https://doi.org/10.9775/kvfd.2009.933
• Javed M., Ahmad I., Usmani N., Ahmad M. (2016). Studies on biomarkers of oxidative stress and associated genotoxicity and histopathology in Channa punctatus from heavy metal polluted canal. Chemosphere, 151:210-219. Doi: https://doi.org/10.1016/j.chemosphere.2016.02.080
• Junianto Z., Apriliani I.M. (2017). Evaluation of heavy metal contamination in various fish meat from Cirata Dam, West Java, Indonesia. AACL Bioflux, 10(2)242-248.
• Kahvecioğlu Ö., Kartal G., Güven A., Timur S. (2003). Metallerin çevresel etkileri-I (environmental effect of metals-I). Metalurji Journal 136:47–53. (in Turkish)
• Karadag H., Fırat Ö., Fırat Ö. (2014). Use of oxidative stress biomarkers in Cyprinus carpio L. for the evaluation of water pollution in Ataturk Dam Lake (Adiyaman, Turkey). Bulletin of Environmental Contamination and Toxicology, 92(3), 289-293. Doi: https://doi.org/10.1007/s00128-013-1187-0
• Kargın F., Erdem C. (1992). Metal accumulation of Tilapia nilotica (L.) in liver, gill and muscle tissues in copper-zinc interaction. Turkish Journal of Zoology, 16:343-348.
• Katalay S., Parlak H., Arslan Ö.Ç. (2005). The accumulation of some heavy metals in the liver tissues of black gobby (Gobius niger L., 1758) living in the aegean sea. Ege University Journal of Fisheries& Aquatic Sciences, 22(3-4):385 – 388. Doi: https://doi.org/10.12714/egejfas.2005.22.3.5000156939
• Kır I., Erdogan M., Engin M. S., Cay S. (2016). Trace metals in sediment, water and their bioaccumalation in Carp (Cyprinus Carpio L., 1758) samples, captured from the Karacaören (I) Dam Lake, Turkey. Fresenius Environmental Bulletin, 35-57. https://www.prt-parlar.de/download_feb_2016
• Köhler A., Deisemann H., Lauritzen B. (1992). Histological and cytochemical indices of toxic injury in the liver of dab Limanda limanda. Marine ecology progress series. 91(1): 141-153. Doi: https://doi.org/10.3354/meps091141
• Kuş U.Ş. (2012). Metazoan parasites of rudd Scardinius erythrophthalmus (Linnaeus, 1758) in lake sapanca. Master’s Thesis, Marmara University. (in Turkish).
• Ledwozyw A., Michalak D., Stepien A., Kadziolka A. (1986). The relationship between plasma triglycerides, cholesterol, total lipids and lipid peroxidation products during human atherosclerosis. Clin Chim Acta, 155(3), 275-283. Doi: https://doi.org/10.1016/0009-8981(86)90247-0
• Mahboob S. (2013). Environmental pollution of heavy metals as a cause of oxidative stress in fish: a review. Life Sci. J, 10, 336-347. http://www.lifesciencesite.com/lsj/life1010s/056_20923life1010s_336_347.pdf
• Mustafa S.A. (2020). Histopathology and heavy metal bioaccumulation in some tissues of Luciobarbus xanthopterus collected from Tigris River of Baghdad, Iraq. The Egyptian Journal of Aquatic Research. In Press. Doi: https://doi.org/10.1016/j.ejar.2020.01.004
• Mwamburi J. (2009). Trace metal concentration in water and sediments of satellite lakes within Lake Victoria. Lakes & Reservoirs: Research & Management, 14(3):203–220. Doi: https://doi.org/10.1111/j.1440-1770.2009.00408.x
• Nammalwar P. (1992). Fish bioassay in the Cooum and Adyar estuaries for environmental management In: Singh KP (ed.). Tropical Ecosystems. Ecology and Management. Wiley Eastern, Delhi. 359–370.
• Okgerman H., Elp M., Dorak Z., Yardımcı H.C., Yılmaz N., Yiğit S. (2006). Changes on the fish fauna of Lake Sapanca. In II National Workshop for Limnology, 6-8.
• Oliveira Ribeiro C.A., Vollaire Y., Sanchez-Chardi A., Roche H. (2005). Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquatic Toxicology, 4:165-171. Doi: https://doi.org/10.1016/j.aquatox.2005.04.008
• Ossana N. A., Baudou F.G., Castañé P.M., Tripoli L., Soloneski S., Ferrari L. (2019). Histological, genotoxic, and biochemical effects on Cnesterodon decemmaculatus (Jenyns 1842) (Cyprinodontiformes, Poeciliidae): early response bioassays to assess the impact of receiving waters. Hindawi Journal of toxicology,1-13. Doi: https://doi.org/10.1155/2019/4687685
• Özyürek F. (2016). Heavy metal accumulation (Cd, Cr, Cu, Fe, Ni, Pb, Zn) in vegetables irrigated with different water resources in Nevşehir. Master’s Thesis, Nevşehir Hacı Bektaşi Veli University. (in Turkish).
• Padmini E., Vijaya Geetha B., Usha Rani M. (2008). Liver oxidative stress of the grey mullet Mugil cephalus presents seasonal variations in Ennore estuary. Brazilian Journal of Medical and Biological Research, 41(11):951-955. DOI: https://doi.org/10.1590/S0100-879X2008005000038
• Pandey S., Parvez S., Sayeed I., Haque R., Bin-Hafeez Raisuddin S. (2003). Biomarkers of oxidative stress: A comparative study of River Yamuna Fish Wallago attu (Bl. & Schn.). The Science of The Total Environment, 309:105- 115. Doi: https://doi.org/10.1016/S0048-9697(03)00006-8
• Pérez-Coyotl I., Galar-Martínez M., García-Medina S., Gómez-Oliván L. M., Gasca-Pérez E., Martínez-Galero E., Islas-Flores H., Pérez-Pastén B.R., Barceló D., López de Alda M.. Pérez-Solsona S., Serra-Roig M.P., Montemurro, N., Peña-Herrera, J.M., Sánchez-Aceves, L. M. (2019). Polluted water from an urban reservoir (Madín dam, México) induces toxicity and oxidative stress in Cyprinus carpio embryos. Environmental pollution, 251, 510-521. Doi: https://doi.org/10.1016/j.envpol.2019.04.095
• Peters N., Köhler A., Kranz H. (1987). Liver pathology in fishes from the lower Elbe as a consequence of pollution. Diseases of Aquatic Organisms, 2:87-97.
• Rajeshkumar S., Liu Y., Ma J., Duan H. Y., Li X. (2017). Effects of exposure to multiple heavy metals on biochemical and histopathological alterations in common carp, Cyprinus carpio L. Fish & shellfish immunology, 70:461-472. Doi: https://doi.org/10.1016/j.fsi.2017.08.013
• Rodrigues R.V., Miranda-Filho K.C., Gusmão E.P., Moreira C.B., Romano L.A., Sampaio L.A. (2010). Deleterious effects of watersoluble fraction of petroleum, diesel and gasoline on marine Pejerrey odontesthesargentinensis Larvae. Science of the Total Environment, 408:2054–2059. DOI: https://doi.org/10.1016/j.scitotenv.2010.01.063
• Şahan A., Kurutaş E.B., Altun T. (2010). The determination of biochemical indicators (biomarkers) in the common carp (Cyprinus carpio) to the physicochemical parameters of the Ceyhan River (Adana-Turkey). Ekoloji, 19:8-14. Doi: https://doi.org/10.5053/ekoloji.2010.762
• Sarkar A., Ray D., Shrivastava A.N. (2006). Molecular Biomarkers: Their significance and application in marine pollution monitoring. Ecotoxicology, 15:333-340. Doi: https://doi.org/10.1007/s10646-006-0069-1
• Sheehan D., Power A. (1999). Effects of seasonality on xenobiotic and antioxidant defence mechanisms of bivalve molluscs. Comp. Biochem. Physiol. 123C:193- 199. Doi: https://doi.org/10.1016/S0742-8413(99)00033-X
• Simonato J.D., Guedes C.L.B., Martinez C.B.R. (2008). Biochemical, physiological, and histological changes in the neotropical fish Prochilodus lineatus exposed to diesel oil. Ecotoxicology and Environmental Safety, 69:112-120. Doi: https://doi.org/10.1016/j.ecoenv.2007.01.012
• Singh A.K., Pathak A.K., Lakra W.S. (2010). Invasion of an exotic fish—common carp, Cyprinus carpio L. (Actinopterygii: Cypriniformes: Cyprinidae) in the Ganga River, India and its impacts. Acta Ichthyol. Piscat. 40 (1): 11-19. Doi: https://doi.org/10.3750/AIP2010.40.1.02
• Şişman I., Imamoglu M., Aydin A. O. (2002). Determination of heavy metals in roadside soil from Sapanca area highway, Turkey. Int. J. Environment and Pollution, 17 (4):306-311. Doi: https://doi.org/10.1504/IJEP.2002.000674
• SKKY, (2004). Regulation on Control of Water Pollution, T.C. Official newspaper, 25687, 31.12.2004.
• Stanley J., Preetha G. (2016). Pesticide toxicity to fishes: exposure, toxicity and risk assessment methodologies. In Pesticide Toxicity to Non-target Organisms (pp. 411-497). Springer, Dordrecht.
• Sümer B., Ileri R., Gezbul H., Senol E. (1996). Investigation of trophic state of the Lake Sapanca. In Symposium on Drinking Water, Istanbul Water and Sewage Administration (ISKI), Istanbul, Turkey. (in Turkish)
• Syasina I. G., Khlopova A.V., Chukhlebova L.M. (2012). Assessment of the state of the gibel carp Carassius auratus gibelio in the Amur River Basin: heavy-metal and arsenic concentrations and histopathology of internal organs. Archives of environmental contamination and toxicology, 62(3):465-478. DOI: https://doi.org/10.1007/s00244-011-9719-2
• Turkey Statistical Institute (TUIK) (2018). Population Projections, 2018-2080. News Bulletin, 30567. https://tuikweb.tuik.gov.tr/PreHaberBultenleri.do?id=30567
• Udroiu L. (2006). The micronucleus test in Piscine erythrocytes. Aquatic Tox., 79:201-204. Doi: https://doi.org/10.1016/j.aquatox.2006.06.013
• Uribe C., Folch H., Enriquez R., Moran G. (2011). Innate and adaptive immunity in teleost fish: a Review. Veterinarni Medicina, 56(10):486-503. Doi: https://doi.org/10.17221/3294-VETMED
• Uysal K. (2010). Heavy metal in edible portions (muscle and skin) and other organs (gill, liver and intestine) of selected freshwater fish Species. International Journal of Food Properties, 14:280-286. Doi: https://doi.org/10.1080/10942910903176378
• Valavanidis A., Vlahogianni T., Dassenakis M., Scoullos M. (2006). Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and environmental safety 64:178-189. Doi: https://doi.org/10.1016/j.ecoenv.2005.03.013
• Yalçın N., Sevinç V. (2001). Heavy metal contents of Lake Sapanca. Turk. J. Chem., 25:521-525. https://journals.tubitak.gov.tr/chem/issues/kim-01-25-4/kim-25-4-16-0010-37.pdf
• Yeşilbudak B., Erdem C. (20149. Cadmium accumulation in gill, liver, kidney and muscle tissues of common carp, Cyprinus carpio, and nile Tilapia, Oreochromis niloticus. Bull. Environ. Contam. Toxicol. 92:546-550. Doi: https://doi.org/10.1007/s00128-014-1228-3
• Yılmaz E. Türkiye’de İçsu Balıkçılığının Mevcut Durumu. Ziraat Mühendisliği, (361), 28-32. https://dergipark.org.tr/en/download/article-file/946517
• Yildirim N.C., Benzer F., Danabas D. (2011). Evaluation of environmental pollution at Munzur River of Tunceli applying oxidative stress biomarkers in Capoeta trutta (Heckel, 1843). The journal of Animal & plant sciences, 21(1):66-71. http://thejaps.org.pk/docs/21(1)2011/EVALUATION-ENVIRONMENTAL.pdf
• Zuo J., Fan W., Wang X., Ren J., Zhang Y., Wang X., Zahnag Y., Yu T., Li X. (2018). Trophic transfer of Cu, Zn, Cd, and Cr, and biomarker response for food webs in Taihu Lake, China. RSC advances, 8(7), 3410-3417. Doi: https://doi.org/10.1039/C7RA11677B