Advertisement

Environmental Science and Pollution Research

, Volume 24, Issue 11, pp 10493–10509 | Cite as

Frequencies of erythrocyte nuclear abnormalities and of leucocytes in the fish Barbus peloponnesius correlate with a pollution gradient in the River Bregalnica (Macedonia)

  • Katerina Rebok
  • Maja Jordanova
  • Valentina Slavevska-Stamenković
  • Lozenka Ivanova
  • Vasil Kostov
  • Trajče Stafilov
  • Eduardo Rocha
Research Article
  • 144 Downloads

Abstract

Integrated chemical and biomarker approaches were performed to estimate if there is ongoing toxicity in the River Bregalnica, namely connected with the presence of metals. The study was performed in water, sediment, and barbel (Barbus peloponnesius), collected in two seasons, from two suspected polluted and one reference zones. The water analyses revealed higher mean values in polluted sites for most of the examined physicochemical parameters. Metal concentrations (Zn, Cu, Cd, Mn, Pb, and Fe) in water were more or less constant, whereas in sediment, they were higher at the two polluted locations. Condition factor (CF), as a general health indicator, revealed better overall condition in barbel from the reference site. In general, blood parameters revealed higher values in the polluted localities. Irrespective of sex and/or season, the frequency of micronuclei (MN) and vacuolated nuclei (VN) were with higher rates in polluted sites. Similarly, the frequencies of the leucocytes (Le), binuclei (BN), and irregularly shaped nuclei (ISN) were also significantly increased in the polluted localities, but they seemed prone to be influenced by sex and/or season. However, strong positive correlations between blood biomarkers and most water physicochemical parameters and metal in sediment were estimated. Our data support that the River Bregalnica’s lower course receives significant genotoxic pollution, likely via metal industry effluents, agricultural runoff, and domestic sewage, and reinforced the utility of MN and other nuclear abnormalities as sensitive and suitable biomarkers for genotoxicity when used in monitoring studies.

Keywords

Blood Fish Genotoxicity Metals Micronuclei Sediment contamination Water quality 

Notes

Acknowledgments

The authors are very thankful to Daniela Jovanovska for making a map for this study. We are also especially thankful to Professor Zlatko Levkov for making the light microscope available that was used for making the digital microphotographs.

References

  1. [APHA] American Public Health Association (1992) Standard methods for the examination of water and wastewater, 18th edn. Washington (DC)Google Scholar
  2. Adhikari S, Sarkar B, Chatterjee A, Mahapatra CT, Ayyappan S (2004) Effects of cypermethrin and carbofuran on certain hematological parameters and prediction of their recovery in a freshwater teleost, Labeo rohita (Hamilton). Ecotox Environ Safe 58:220–226CrossRefGoogle Scholar
  3. AI-Sabti K, Metcalfe CD (1995) Fish micronuclei for assessing genotoxicity in water. Mutat Res 343:121–135CrossRefGoogle Scholar
  4. Ali FK, El-Shehawi AM, Seehy MA (2008) Micronucleus test in fish genome: a sensitive monitor for aquatic pollution. Afr J Biotech 7(5):606–612Google Scholar
  5. Andreevska D, Menkovska M, Andov D (2013) Overview of the current condition, in production, consumption and the research potential of the rice crop in the Republic of Macedonia. Macedonian J Anim Sci 3(2):219–228Google Scholar
  6. Ates B, Orun I, Talas ZS, Durmaz G, Yilmaz I (2007) Effects of sodium selenite on some biochemical and hematological parameters of rainbow trout (Oncorhynchus mykiss Walbaum, 1792) exposed to Pb2+ and Cu2+. Fish Physiol Biochem 34(1):53–59CrossRefGoogle Scholar
  7. Ayllón F, Garcia-Vazquez E (2000) Induction of micronuclei and other nuclear abnormalities in European minnow Phoxinus phoxinus and mollie Poecilia latipinna: an assessment of the fish micronucleus test. Mutat Res 467:177–186CrossRefGoogle Scholar
  8. Balabanova B, Stafilov T, Šajn R, Bačeva K (2011) Distribution of chemical elements in attic dust as reflection of lithology and anthropogenic influence in the vicinity of copper mine and flotation. Arch Environ Contam Toxicol 61(2):173–184CrossRefGoogle Scholar
  9. Balabanova B, Stafilov T, Šajn R, Bačeva K (2013) Spatial distribution and characterization of some toxic metals and lithogenic elements in topsoil and subsoil from copper mine environs. Int J Environ Prot 3(9):1–9Google Scholar
  10. Barišić J, Dragun Z, Ramani S, Filipović Marijić V, Krasnići N, Čož-Rakovac R, Kostov V, Rebok K, Jordanova M (2015) Evaluation of histopathological alterations in the gills of Vardar chub (Squalius vardarensis Karaman) as an indicator of river pollution. Ecotox Environ Safe 118:158–166CrossRefGoogle Scholar
  11. Baršiené J, Butrimavičiené L, Michailovas A, Grygiel W (2015) Assessing the environmental genotoxicity risk in the Baltic Sea: frequencies of nuclear buds in blood erythrocytes of three native fish species. Environ Monit Assess 187(1):4078. doi: 10.1007/s10661-014-4078-x CrossRefGoogle Scholar
  12. Baršiené J, Dedonytė V, Rybakovas A, Andreikėnaitė L, Andersen OK (2006) Investigation of micronuclei and other nuclear abnormalities in peripheral blood and kidney of marine fish treated with crude oil. Aquat Toxicol 785:599–5104Google Scholar
  13. Boettcher M, Grund S, Keiter S, Kosmehl T, Reifferscheid G, Seitz N, Rocha PS, Hollert H, Braunbeck T (2010) Comparison of in vitro and in situ genotoxicity in the Danube River by means of the comet assay and the micronucleus test. Mutat Res Gen Toxicol Environ Mutagen 700(1–2):11–17CrossRefGoogle Scholar
  14. Carballo M, Jiménez JA, de la Torre A, Roset J, Muñoz MJ (2004) A survey of potential stressor-induced physiological changes in carp (Cyprinus carpio) and barbel (Barbus bocagei) along the Tajo River. Environ Toxicol 20(2):119–125CrossRefGoogle Scholar
  15. Carrasco K, Tilbury KL, Myers MS (1990) Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Can J Fish Aquat Sci 47:2123–2136CrossRefGoogle Scholar
  16. Carrola J, Santos N, Rocha MJ, Fontainhas-Fernandes A, Pardal MA, Monteiro RA, Rocha E (2014) Frequency of micronuclei and of other nuclear abnormalities in erythrocytes of the grey mullet from the Mondego, Douro and Ave estuaries—Portugal. Environ Sci Pollut Res Int 21(9):6057–6068CrossRefGoogle Scholar
  17. Çavaş T, Ergene-Gözükara S (2003) Evaluation of the genotoxic potential of lambda-cyhalothrin using nuclear and nucleolar biomarkers on fish cells. Mutat Res 534:93–99CrossRefGoogle Scholar
  18. Çavaş T, Ergene-Gözükara S (2005) Micronucleus test in fish cells: a bioassay for in situ monitoring of genotoxic pollution in the marine environment. Environ Mol Mutagen 46:64–70CrossRefGoogle Scholar
  19. CEN EN 14011:2003 Water analysis—fishing with electricity for wadable and non-wadable rivers. European Committee for StandardizationGoogle Scholar
  20. Costa PM, Lobo J, Caeiro S, Martins M, Ferreira AM, Caetano M, Vale C, DelValls Á, Costa MH (2008) Genotoxic damage in Solea senegalensis exposed to sediments from the Sado Estuary (Portugal): effects of metallic and organic contaminants. Mutat Res 654:29–37CrossRefGoogle Scholar
  21. Das BK, Mukherjee SC (2003) Toxicity of cypermethrin in Labeo rohita fingerlings: biochemical, enzymatic and haematological consequences. Comp Biochem Physiol C 134:109–121Google Scholar
  22. Dimitrovska O, Markoski B, Apostolovska Toshevska B, Milevski I, Gorin S (2012) Surface water pollution of major rivers in the Republic of Macedonia. Procedia Environ Sci 14:32–40CrossRefGoogle Scholar
  23. Ergene S, Çavaş T, Çelik A, Köleli N, Kaya F, Karahan A (2007) Monitoring of nuclear abnormalities in peripheral erythrocytes of three fish species from the Goksu Delta (Turkey): genotoxic damage in relation to water pollution. Ecotoxicology 16:385–391CrossRefGoogle Scholar
  24. Facey DE, Blazer VS, Gasper MM, Turcotte CL (2005) Using fish biomarkers to monitor improvements in environmental quality. J Aquat Anim Health 17:263–266CrossRefGoogle Scholar
  25. Fuzinatto CF, Flohr L, Melegari SP, Matias WG (2013) Induction of micronucleus of Oreochromis niloticus exposed to waters from the Cubatão do Sul River, southern Brazil. Ecotox Environ Safe 98:103–109CrossRefGoogle Scholar
  26. George-Nascimento M, Khan RA, Garcias F, Lobes V, Murñoz G, Valdebenito V (2000) Impaired health in flounder, Paralichthys spp. inhabiting coastal Chile. Bull Environ Contam Toxicol 64:184–190CrossRefGoogle Scholar
  27. Georgiev S (1998) Key for determination of fish (Osteichthyes) and cephalospidomorphs (Cephalaspidomorpha) from R. Macedonia. Institute of Animal Sciences, Skopje, p 178 (in Macedonian)Google Scholar
  28. Guijarro AI, Lopez-Patinõ MA, Pinillos ML, Isorna E, De Pedro N, Alonso-Gomez A-BM, Delgado MJ (2003) Seasonal changes in haematology and metabolic resources in the tench. J Fish Biol 62:803–815CrossRefGoogle Scholar
  29. Huges JB, Hebert AT (1991) Erythrocyte micronuclei in winter flounder (Pseudopleuronectes americanus): results of field surveys during 1980-1988 from Virginia to Nova Scotia and in Long Island Sound. Arch Environ Contam Toxicol 20:474–479CrossRefGoogle Scholar
  30. Ilić Popov S, Stafilov T, Šajn R, Tánáselia C, Bačeva K (2014) Applying of factor analyses for determination of trace elements distribution in water from river Vardar and its tributaries, Macedonia/Greece. Sci World J Article ID 809253:1–11. doi: 10.1155/2014/809253 Google Scholar
  31. Jordanova M, Rebok K, Dragun Z, Ramani S, Ivanova L, Kostov V, Valić D, Krasnići N, Filipović Marijić V, Kapetanović D (2016) Histopathology investigation on the Vardar chub (Squalius vardarensis) populations captured from the rivers impacted by mining activities. Ecotox Environ Safe 129:35–42CrossRefGoogle Scholar
  32. Joshi BD (1980) Sex-related variations in some haematologic values of certain freshwater teleosts. Japanese J Ichthyol 27(2):139–143Google Scholar
  33. Kavadias S, Castritsi-Catharios J, Dessypris A, Milious H (2004) Seasonal variation in steroid hormones and blood parameters in cage-farmed European sea bass (Dicentrarchus labrax L.) J Appl Ichthyol 20:58–63CrossRefGoogle Scholar
  34. Koca YB, Koca S, Yildiz Ş, Gürcü B, Osanç E, Tunçbaş O, Aksoy G (2005) Investigation of histopathological and cytogenetic effects on Lepomis gibbosus (Pisces: Perciformes) in the Çine stream (Aydın/Turkey) with determination of water pollution. Environ Toxicol 20(6):560–571CrossRefGoogle Scholar
  35. Kori-Siakpere O, Ake JEG, Idoge E (2005) Haematological characteristics of the African snakehead, Parachanna obscura. Afr J Biotechnol 4(6):527–530Google Scholar
  36. Kostov V, Rebok K, Slavevska-Stamenković V, Ristovska M (2010) Fish fauna of River Bregalnica (R. Macedonia)—composition, abundance and longitudinal distribution. Conference BALWOIS 2010. Proceedings of papers. Topics 6 Lakes and Wetlands, 1–8Google Scholar
  37. Kumar S, Lata S, Gopal K (1999) Deltamethrin induced physiological changes in freshwater cat fish Heteropneustes fossilis. Bull Environ Contam Toxicol 62:254–258CrossRefGoogle Scholar
  38. Leary S, Underwood W, Anthony R, Cartner S, Corey D, Grandin T, Greenacre C, Gwaltney-Brant S, McCrackin MA, Meyer R, Miller D, Shearer J, Yanong R (2013) AVMA guidelines for the euthanasia of animals: 2013 edition. American Veterinary Medical Association, Schaumburg, ILGoogle Scholar
  39. Li S, Li J, Zhang Q (2011) Water quality assessment in the rivers along the water conveyance system of the Middle Route of the South to North Water Transfer Project (China) using multivariate statistical techniques and receptor modeling. J Hazard Mat 195:306–317CrossRefGoogle Scholar
  40. Liu N, Ma M, Xu Y, Zha J, Rao K, Wang Z (2013) Susceptibility of male and female Japanese medaka (Oryzias latipes) to 2,4,6-trichlorophenol-induced micronuclei in peripheral erythrocytes. Front Environ Sci Eng 7(1):77–84CrossRefGoogle Scholar
  41. Maceda-Veiga A, Monroy M, Viscor G, De Sostoa A (2010) Changes in non-specific biomarkers in the Mediterranean barbel (Barbus meridionalis) exposed to sewage effluents in a Mediterranean stream (Catalonia, NE Spain). Aquat Toxicol 100:229–237CrossRefGoogle Scholar
  42. Mazon AF, Monteiro EAS, Pinheiro GHD, Fernandes MN (2002) Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish, Prochilodus scrofa. Braz J Biol 62(4A):621–631CrossRefGoogle Scholar
  43. Mekkawey IA, Mahmoud UM, Sayed AEH (2011) Effects of 4-nonylphenol on blood cells of the African catfish Clarias gariepinus (Burchell, 1822). Tiss Cell 43:223–229CrossRefGoogle Scholar
  44. Mgbenka BO, Oluah NS, Arungwa AA (2005) Erythropoietic response and hematological parameters in the catfish Clarias albopunctatus exposed to sublethal concentrations of actellic. Ecotoxicol Environ Safe 62:436–440CrossRefGoogle Scholar
  45. Milevski I, Blinkov I, Trendafilov A (2008) Soil erosion processes and modeling in the upper Bregalnica catchment. XXIVth Conference of Danubian Countries on the Hydrological Forecasting and Hydrological Bases of Water Management, Bled, Slovenia, Proceedings 1–10Google Scholar
  46. Minissi S, Ciccotti E, Rizzoni M (1996) Micronucleus test in erythrocytes of Barbus plebejus (Teleostei, Pisces) from two natural environments: a bioassay for the in situ detection of mutagens in freshwater. Mutat Res 367:245–251CrossRefGoogle Scholar
  47. Muranli FDG, Güner U (2011) Induction of micronuclei and nuclear abnormalities in erythrocytes of mosquito fish (Gambusia affinis) following exposure to the pyrethroid insecticide lambda-cyhalothrin. Mutat Res Genet Toxicol Environ Mutagen 726:104–108CrossRefGoogle Scholar
  48. Nikoo M, Falahatkar B, Rahmani H (2010) Blood parameters of Southern Caspian kutum Rutilus kutum. J Appl Ichthyol:1–3. doi: 10.1111/j.1439-0426.2010.01588.x
  49. Nussey G, Van Vuren JHJ, Du Preez HH (1995) Effect of copper on blood coagulation of Oreochromis mossambicus (Cichlidae). Comp Biochem Physiol C 111:359–367Google Scholar
  50. Osman A, Ali E, Hashem M, Mostafa M, Mekkawy I (2010) Genotoxicity of two pathogenic strains of zoosporic fungi (Achlya klebsiana and Aphanomyces laevis) on erythrocytes of Nile tilapia Oreochromis niloticus niloticus. Ecotoxicol Environ Safe 73:24–31CrossRefGoogle Scholar
  51. Ossana NA, Salibián A (2013) Micronucleus test for monitoring the genotoxic potential of the surface water of Luján River (Argentina) using erythrocytes of Lithobates catesbeianus tadpoles. Ecotoxicol Environ Contam 8(1):67–74. doi: 10.5132/eec.2013.01.010 Google Scholar
  52. Pavlidis M, Futter W, Katharios P, Divanach P (2007) Blood cell profile of six Mediterranean mariculture fish species. J Appl Ichthyol 23:70–73CrossRefGoogle Scholar
  53. Pierson PM, Lamers A, Flik G, Mayer-Gostan N (2004) The stress axis, stanniocalcin, and ion balance in rainbow trout. Gen Comp Endocrinol 137:263–271CrossRefGoogle Scholar
  54. Ramani S, Dragun Z, Kapetanović D, Kostov V, Jordanova M, Erk M, Hajrulai-Musliu Z (2014) Surface water characterization of three rivers in the lead/zinc mining region of northeastern Macedonia. Arch Environ Contam Toxicol 66:514–528CrossRefGoogle Scholar
  55. Regulation for Water Classification and Regulation for categorization of Watercourses, Lakes, Accumulations and Underground waters (1999) Official Gazette of Republic of Macedonia 18/99Google Scholar
  56. Rocha E, Rocha JM, Galante HM, Silva WM, Monteiro AFR (2009) The hepatocytes of the brown trout (Salmo trutta F. fario): a stereological study of their number and size during the breeding cycle. Ichthyol Res 56:43–54CrossRefGoogle Scholar
  57. Santos AA, Egami MI, Ranzani-Paiva MJT, Juliano Y (2009) Hematological parameters and phagocytic activity in fat snook (Centropomus parallelus): seasonal variation, sex and gonadal maturation. Aquaculture 296:359–366CrossRefGoogle Scholar
  58. Serafimovska JM, Arpadjan S, Stafilov T, Popov IS (2011) Dissolved inorganic antimony, selenium and tin species in water samples from various sampling sites of river Vardar in Macedonia and Greece. Maced J Chem Chem Eng 30(2):181–188Google Scholar
  59. Singh NN, Srivastava AK (2010) Haematological parameters as bioindicators of insecticide exposure in teleosts. Ecotoxicol 19:838–854CrossRefGoogle Scholar
  60. Šorić V (1992) The structure of population and reproductive potential of Barbus peloponnesius petenyi (Cyprinidae, Pisces) in the Gruza River. Collection of Scientific Papers, Faculty of Science Kragujevac 13:65–75 (In Serbian)Google Scholar
  61. Šorić V, Janković D (1989) Characteristics of growth and sexual maturity of Barbus meridionalis. Ichthyologia 21(1):27–37 (In Serbian)Google Scholar
  62. Srivastava AK, Mishra J (1983) Effects of fenthion on the blood and tissue chemistry of a teleost fish (Heteropneustes fossilis). J Comp Path 93:27–31CrossRefGoogle Scholar
  63. Stafilov T, Peeva L, Nikov B, De Koning A (2009) Industrial hazardous waste in the Republic of Macedonia. Applied environmental geochemistry—anthropogenic impact on human environment in the SE Europe, Ljubljana, Proceedings Book, Šajn R, Žilbert G, Alijagić J (ed), ISBN 978–961-6498-18-0. 108–112Google Scholar
  64. Stipaničev D, Dragun Z, Repec S, Rebok K, Jordanova M (2017) Broad spectrum screening of 463 organic contaminants in rivers in Macedonia. Ecotoxicol Environ Safe 135:48–59CrossRefGoogle Scholar
  65. Strunjak-Perovic I, Coz-Rakovac R, Topic Popovic N, Jadan M (2008) Seasonality of nuclear abnormalities in gilthead sea bream Sparus aurata (L.) erythrocytes. Fish Physiol Biochem 35(2):287–291CrossRefGoogle Scholar
  66. Tierney KB, Farrell AP, Kennedy CJ (2004) The differential leucocyte landscape of four teleosts: juvenile Oncorhynchus kisutch, Clupea pallasi, Culaea inconstans and Pimephales promelas. J Fish Biol 65:906–919CrossRefGoogle Scholar
  67. Vasiliou A, Economidis PS (2005) On the life-history of Barbus peloponnesius and Barbus cyclolepis in Macedonia, Greece. Folia Zool 54(3):316–336Google Scholar
  68. Vázquez GR, Guerrero GA (2007) Characterization of blood cells and hematological parameters in Cichlasoma dimerus (Teleostei, Perciformes). Tiss Cell 39:151–160CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Institute of Biology, Faculty of Natural Sciences and Mathematics“Ss Cyril and Methodius” UniversitySkopjeRepublic of Macedonia
  2. 2.Fisheries DepartmentInstitute of Animal ScienceSkopjeRepublic of Macedonia
  3. 3.Institute of Chemistry, Faculty of Natural Sciences and Mathematics“Ss Cyril and Methodius” UniversitySkopjeRepublic of Macedonia
  4. 4.Laboratory of Histology and Embryology, Department of Microscopy, Institute of Biomedical Sciences Abel Salazar (ICBAS)University of Porto (UPorto)PortoPortugal
  5. 5.Group of Histomorphology, Physiopathology and Applied Toxicology, Interdisciplinary Center of Marine and Environmental Research (CIIMAR/CIMAR)University of Porto (UPorto)MatosinhosPortugal

Personalised recommendations