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HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS

Yıl 2020, Cilt: 9 Sayı: 2, 169 - 178, 30.07.2020
https://doi.org/10.18036/estubtdc.653015

Öz

In this study, the chromosomal aberrations were investigated for the first time in the subterranean Nannospalax xanthodon species. The sites in Bilecik province where the samples were collected was divided into the metal-polluted and non-polluted area. The concentrations of cadmium, copper, nickel, lead, and zinc were measured on the Atomic Absorption Spectrometer in the soil samples and liver tissues of the animals. The metal levels detected in liver tissues were found to be higher than the metal levels of soil samples. Therefore, it has been revealed that the Nannospalax species are appropriate biomonitors for the determination of terrestrial pollution. The examination of chromosomes revealed intense deletions and fragmentations in the chromosome plates of samples from the polluted group. It has been shown that these chromosome aberrations can be associated with metal pollution.

Kaynakça

  • [1] Dubovskiy IM, Grizanova EV, Ershova NS, Rantala MJ, Glupov VV. The effects of dietary nickel on the detoxification enzymes, innate immunity and resistance to the fungus Beauveria bassiana in the larvae of the greater wax moth Galleria mellonella. Chemosphere 2011; 85:92-96.
  • [2] Sánchez-Chardi A, Ribeiro CAO, Nadal J. Metals in liver and kidneys and the effects of chronic exposure to pyrite mine pollution in the shrew Crocidura russula inhabiting the protected wetland of Doñana. Chemosphere 2009; 76:387-394.
  • [3] Marschner H. Mineral Nutrition of Higher Plants. London:Academic Press, 1995, pp. 299-312.
  • [4] Smith PN, Cobb GP, Godard-Codding C, Hoff D, McMurry ST, Rainwater TR, Reynolds KD. Contaminant exposure in terrestrial vertebrates. Environ Pollut 2007; 150:41-64.
  • [5] Talmage SS, Walton BT. Small mammals as monitors of environmental contaminants. Rev Environ Con Tox 1991; 119; 47–145.
  • [6] Sözen M. A biological investigation on Turkish Spalax Güldenstaedt, 1770 (Mammalia: Rodentia). GU J Sci 2005; 2:167-181.
  • [7] Yağcı T, Coşkun Y, Aşan N. Tunnel structure of blind mole rats (genus Nannospalax) in Turkey (Rodentia: Spalacidae).Zool. in the Mid. East 2010; 50: 35-40.
  • [8] Sharma N, Trikha P, Akhtar M, Raisuddin S. Inhibitory effect of Emblica officinalis on the in vivo clastogenicity of benzo[a]pyrene and cyclophosphamide in mice. Hum Exp Toxicol 2000; 22:643–653.
  • [9] Antonelli A, Portesi A, Cozzi E, Tradanico A, Bbalzarini R, Grigoloto P, Cosciani-Cunico PG. The collecting duct carcinoma of the kidney: a cytogenetical study. Eur Urol 2003; 43:680–685.
  • [10] Topashka-Ancheva M, Metcheva R, Teodorovab S. A comparative analysis of the heavy metal loading of small mammals in different regions of Bulgaria II: chromosomal aberrations and blood pathology. Ecotoxicol Environ Saf 2003; 54:188-193.
  • [11] Agarwal KA, Sharma A, Talukder G. Clastogenic effects of copper sulphate on the bone marrow chromosomes of mice in vivo. Mutation Research 1990; 243:1-6.
  • [12] Nehez M, Lorencz R, Desi I. Simultaneous Action of Cypermethrin and Two Environmental Pollutant Metals, Cadmium and Lead, on Bone Marrow Cell Chromosomes of Rats in Subchronic Administration. Ecotoxicol Environ Saf 2000; 45:55-60.
  • [13] Mertens J, Luyssaert S, Verbeeren S, Vervaeke P, Lust N. Cd and Zn concentrations in small mammals and willow leaves on disposal facilities for dredged material. Environ Pollut 2001;115:17-22.
  • [14] Sanchez-Chardi A, Lopez-Fuster MJ, Nadal J. Bioaccumulation of lead, mercury, and cadmium in the greater white-toothed shrew, Crocidura russula, from the Ebro Delta (NE Spain): sex- and age-dependent variation. Environ Pollut 2007a; 145:7-14.
  • [15] Sanchez-Chardi A, Marques CC, Nadal J, Mathias ML. Metal bioaccumulation in the greater white-toothed shrew, Crocidura russula, inhabiting an abandoned pyrite mine site. Chemosphere 2007b; 67:121-130.
  • [16] Yağcı T, Aşan N. A live trap model for subterranean mole rats. Mammalia 2007; 71:98-99.
  • [17] Beernaert J, Scheirs J, Den Brande VG, Leirs H, Blust R, De Meulenaer B, Camp VJ, Verhagen R. Do wood mice (Apodemus sylvaticus) use food selection as a means to reduce heavy metal intake?. Environ Pollut 2008; 151:599-607.
  • [18] Ajayi OA, Idowu, AB, Eromosele CO, Dedeke GA, Ademolu KO. Distribution and Effect of some Heavy Metals in Selected Organs and Tissues of Albino Rats Exposed to Vehicular Exhaust Fumes. Proceedings of the Environmental Management Conference, Federal University of Agriculture, Abeokuta, Nigeria, 2011, pp. 519-526
  • [19] Ford CE, Hamerton JL. A colchicine, hypotonic citrate, squash sequence for mammalian chromosomes. Stain Technol 1956; 31:247–251. [20] El-Refaiy AI, Eissa FI. Histopathology and cytotoxicity as biomarkers in treated rats with cadmium and some therapeutic agents.Saudi J Biol Sci 2013; 20:265–280.
  • [21] Aly FM, Kotb AM, Seddik H. Effects of Spirulina platensis on DNA damage and chromosomal aberration against cadmium chloride-induced genotoxicity in rats. Environ Sci Pollut Res 2018; 11:829-836.
  • [22] Turkish Environmental Legislation: Regulations, Regulation on Control of Soil Pollution (Official Gazatte dated 31.05.2005 and no. 25831).
  • [23] Regulations on Using Domestic and Urban Treatment Sludges within Soil (Official Gazette dated 03.08.2010 and no. 27661)
  • [24] Benavides MP, Gallego SM, Tomaro LM. Cadmium tox icity in plants. Braz J Plant Physiol 2005; 17:21–34.
  • [25] ECDGE, European Commission Director General Environment. Heavy metals and organic compounds from wastes used as organic fertilizers. Final Report. July WPA Consulting Engineers İnc, 2010.
  • [26] Viard B, Pihan F, Promeyrat S, Pihan J. Integrated Assessment of heavy metal (Pb, Zn, Cd) highway pollution:bioaccumulation in soil, Graminaceae and Land Snails. Chemosphere 2004; 55:1349-1359.
  • [27] Çelik A, Kartal AA, Akdoğan A, Kaska Y. Determining the heavy metal pollution in Denizli (Turkey) by using Robinia pseudo-acacia L. Environ. Int 2005; 31: 105-112.
  • [28] Vidhya L, Dhandapani M, Sekar M, Mahimairaja S. Lead pollution in soil, water and plants due to automobile emission in urban environments in Coimbatore. Madras Agric. J 2007;94: 89-96.
  • [29] Viegas-Crespo AM, Lopes PA, Pinheiro MT, Santos MC, Rodrigues PD, Nunes AC, Marques C, Mathias ML.Hepatic elemental contents and antioxidant enzyme activities in Algerian mice (Mus spretus) inhabiting a mine area in central Portugal.Sci. Total Environ 2003; 311: 101–109.
  • [30] Schleich CE, Beltrame MO, Carlos DA. Heavy metals accumulation in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae) from areas with different risk of contamination'. Folia Zool 2010; 2:108-114.
  • [31] Lourenço J, Pereira R, Gonçalves F, Mendo S. Metal bioaccumulation, genotoxicity and gene expression in the European wood mouse (Apodemus sylvaticus) inhabiting an abandoned uranium mining area. Sci. Total Environ 2013; 443:673–680.
  • [32] Arslan A, Kryštufek B, Matur F, Zima J. Review of chromosome races in blind mole rats (Spalax and Nannospalax). Folia Zool 2016; 4:249-301.
  • [33] Yağcı T. C- and NOR-banding karyotype analysis of Nannospalax xanthodon (2n=52, 2n=60) and new locality for 2n=52 cytotype from western Anatolia. Caryologia 2017; 71:7-12.
  • [34] SETAC-Society of Environmental Toxicology and Chemistry. Environmental contaminants in wildlife: interpreting tissue concentrations, in: W.N. Beyer, G.H. Heinz, A.W. Redmon-Norwood (Eds.), CRC Lewis, Boca Raton, 1996, 494 pp.
  • [35] Freedman B. Toxic elements, in: B. Freedman (Ed.), Environmental Ecology: The Ecological Effects of Pollution, Disturbance, and Other Stresses, Academic Press, London, 1995, pp. 62-93.
  • [36] Silva J, TRO Freitas, Heuser V, Marinho JR, Bittencourt F, Tadeu C, Cerski S, Kliemann LM, Erdtmann B. Effects of chronic exposure to coal in wild rodents (Ctenomys torquatus) evaluated by multiple methods and tissues. Mutation Research 2000; 470:39-51.
  • [37] Smith GJ, Rongstad OJ. Small mammal heavy metal concentrations from mined and control sites. Environ Pollut 1982; 28:121-134.
  • [38] Pankakoski E, Koivisto I, Hyvarinen H, Terhivuo J. Shrews as indicators of heavy metal pollution. Carnegie Museum Nat Hist Spec Publ. 1994; 18, 137–149.
  • [39] Komarnicki GJK. Tissue, sex and age specific accumulation of heavy metals (Zn, Cu, Pb, Cd) by populations of the mole (Talpa europaea L.) in a central urban area. Chemosphere 2000; 41:1593–1602.
  • [40] Lopes PA, Viegas-Crespo AM, Nunes AC, Pinheiro T, Marques C, Santos MA, Mathias ML. Influence of age, sex, and sexual activity on trace element levels and antioxidant enzyme activities in field mice (Apodemus sylvaticus and Mus spretus). Biol Trace Elem Res 2002; 85:227-239.
  • [41] Singh P, Sankhla V. In situ protective effect of curcumin on cadmium chloride induced genotoxicity in bone marrow chromosomes of Swiss albino mice. J Cell Mol Biol 2010; 2: 57-64.
  • [42] Jihen EH, Imed M, Fatima H, Abdelhamid K. Protective effects of selenium (Se) and zinc (Zn) on cadmium (Cd) toxicity in the liver of the rat: effects on the oxidative stress. Ecotoxicol Environ Saf 2009; 5:1559-1564.
  • [43] Jemai H, Lachkar HA, Messaoudi I, Kerkeni A. Effect of zinc pre-treatment on blood glutathione, serum zinc and kidney histological organization in male rats exposed to cadmium. J Trace Elem Med Bıo 2010; 4:277-288.
  • [44] Nevo E. Stress, adaptation, and speciation in the evolution of the blind mole rat, Spalax, in Israel. Mol. Phylogenetics Evol 2013; 66:515–525.
  • [45] Savic I, Nevo E.The Spalacidae; Evolutionary history, speciation and population biology, in; Evolution of Subterranean Mammals at the Organismal and Molecular Levels. Alan R. Liss New York: pp.129-153.
  • [46] Nevo E, Filippucci MG, Redi C, Korol A, Beiles A. Chromosomal speciation and adaptive radiation of mole rats in Asia Minor correlated with increased ecological stress. Proc Natl Acad Sci 1994b; 91: 8160-8164.
  • [47] Nevo E, Filippucci MG, Redi C, Simson S, Heth G, Beiles A. Karyotype and genetic evolution in speciation of subterranean mole rats of the genus Spalax in Turkey. Biol J Linn Soc 1995; 54: 203-229.

HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS

Yıl 2020, Cilt: 9 Sayı: 2, 169 - 178, 30.07.2020
https://doi.org/10.18036/estubtdc.653015

Öz

In this preliminary study, the chromosomal aberrations were investigated for the first time in the subterranean Nannospalax xanthodon species. The locations in Bilecik province where the samples were collected were divided into the polluted and non-polluted area. The concentrations of cadmium, copper, nickel, lead, and zinc were measured on the Atomic Absorption Spectrometer in the soil samples and liver tissues of the animals. The metal levels detected in liver tissues were found to be higher than the metal levels of soil samples. Therefore, Nannospalax species were considered as appropriate bioindicators for the determination of terrestrial pollution. The examination of chromosomes revealed intense deletions and fragmentations in the chromosome plates of samples from the polluted area. It was concluded that these chromosome aberrations can be associated with metal pollution.

Kaynakça

  • [1] Dubovskiy IM, Grizanova EV, Ershova NS, Rantala MJ, Glupov VV. The effects of dietary nickel on the detoxification enzymes, innate immunity and resistance to the fungus Beauveria bassiana in the larvae of the greater wax moth Galleria mellonella. Chemosphere 2011; 85:92-96.
  • [2] Sánchez-Chardi A, Ribeiro CAO, Nadal J. Metals in liver and kidneys and the effects of chronic exposure to pyrite mine pollution in the shrew Crocidura russula inhabiting the protected wetland of Doñana. Chemosphere 2009; 76:387-394.
  • [3] Marschner H. Mineral Nutrition of Higher Plants. London:Academic Press, 1995, pp. 299-312.
  • [4] Smith PN, Cobb GP, Godard-Codding C, Hoff D, McMurry ST, Rainwater TR, Reynolds KD. Contaminant exposure in terrestrial vertebrates. Environ Pollut 2007; 150:41-64.
  • [5] Talmage SS, Walton BT. Small mammals as monitors of environmental contaminants. Rev Environ Con Tox 1991; 119; 47–145.
  • [6] Sözen M. A biological investigation on Turkish Spalax Güldenstaedt, 1770 (Mammalia: Rodentia). GU J Sci 2005; 2:167-181.
  • [7] Yağcı T, Coşkun Y, Aşan N. Tunnel structure of blind mole rats (genus Nannospalax) in Turkey (Rodentia: Spalacidae).Zool. in the Mid. East 2010; 50: 35-40.
  • [8] Sharma N, Trikha P, Akhtar M, Raisuddin S. Inhibitory effect of Emblica officinalis on the in vivo clastogenicity of benzo[a]pyrene and cyclophosphamide in mice. Hum Exp Toxicol 2000; 22:643–653.
  • [9] Antonelli A, Portesi A, Cozzi E, Tradanico A, Bbalzarini R, Grigoloto P, Cosciani-Cunico PG. The collecting duct carcinoma of the kidney: a cytogenetical study. Eur Urol 2003; 43:680–685.
  • [10] Topashka-Ancheva M, Metcheva R, Teodorovab S. A comparative analysis of the heavy metal loading of small mammals in different regions of Bulgaria II: chromosomal aberrations and blood pathology. Ecotoxicol Environ Saf 2003; 54:188-193.
  • [11] Agarwal KA, Sharma A, Talukder G. Clastogenic effects of copper sulphate on the bone marrow chromosomes of mice in vivo. Mutation Research 1990; 243:1-6.
  • [12] Nehez M, Lorencz R, Desi I. Simultaneous Action of Cypermethrin and Two Environmental Pollutant Metals, Cadmium and Lead, on Bone Marrow Cell Chromosomes of Rats in Subchronic Administration. Ecotoxicol Environ Saf 2000; 45:55-60.
  • [13] Mertens J, Luyssaert S, Verbeeren S, Vervaeke P, Lust N. Cd and Zn concentrations in small mammals and willow leaves on disposal facilities for dredged material. Environ Pollut 2001;115:17-22.
  • [14] Sanchez-Chardi A, Lopez-Fuster MJ, Nadal J. Bioaccumulation of lead, mercury, and cadmium in the greater white-toothed shrew, Crocidura russula, from the Ebro Delta (NE Spain): sex- and age-dependent variation. Environ Pollut 2007a; 145:7-14.
  • [15] Sanchez-Chardi A, Marques CC, Nadal J, Mathias ML. Metal bioaccumulation in the greater white-toothed shrew, Crocidura russula, inhabiting an abandoned pyrite mine site. Chemosphere 2007b; 67:121-130.
  • [16] Yağcı T, Aşan N. A live trap model for subterranean mole rats. Mammalia 2007; 71:98-99.
  • [17] Beernaert J, Scheirs J, Den Brande VG, Leirs H, Blust R, De Meulenaer B, Camp VJ, Verhagen R. Do wood mice (Apodemus sylvaticus) use food selection as a means to reduce heavy metal intake?. Environ Pollut 2008; 151:599-607.
  • [18] Ajayi OA, Idowu, AB, Eromosele CO, Dedeke GA, Ademolu KO. Distribution and Effect of some Heavy Metals in Selected Organs and Tissues of Albino Rats Exposed to Vehicular Exhaust Fumes. Proceedings of the Environmental Management Conference, Federal University of Agriculture, Abeokuta, Nigeria, 2011, pp. 519-526
  • [19] Ford CE, Hamerton JL. A colchicine, hypotonic citrate, squash sequence for mammalian chromosomes. Stain Technol 1956; 31:247–251. [20] El-Refaiy AI, Eissa FI. Histopathology and cytotoxicity as biomarkers in treated rats with cadmium and some therapeutic agents.Saudi J Biol Sci 2013; 20:265–280.
  • [21] Aly FM, Kotb AM, Seddik H. Effects of Spirulina platensis on DNA damage and chromosomal aberration against cadmium chloride-induced genotoxicity in rats. Environ Sci Pollut Res 2018; 11:829-836.
  • [22] Turkish Environmental Legislation: Regulations, Regulation on Control of Soil Pollution (Official Gazatte dated 31.05.2005 and no. 25831).
  • [23] Regulations on Using Domestic and Urban Treatment Sludges within Soil (Official Gazette dated 03.08.2010 and no. 27661)
  • [24] Benavides MP, Gallego SM, Tomaro LM. Cadmium tox icity in plants. Braz J Plant Physiol 2005; 17:21–34.
  • [25] ECDGE, European Commission Director General Environment. Heavy metals and organic compounds from wastes used as organic fertilizers. Final Report. July WPA Consulting Engineers İnc, 2010.
  • [26] Viard B, Pihan F, Promeyrat S, Pihan J. Integrated Assessment of heavy metal (Pb, Zn, Cd) highway pollution:bioaccumulation in soil, Graminaceae and Land Snails. Chemosphere 2004; 55:1349-1359.
  • [27] Çelik A, Kartal AA, Akdoğan A, Kaska Y. Determining the heavy metal pollution in Denizli (Turkey) by using Robinia pseudo-acacia L. Environ. Int 2005; 31: 105-112.
  • [28] Vidhya L, Dhandapani M, Sekar M, Mahimairaja S. Lead pollution in soil, water and plants due to automobile emission in urban environments in Coimbatore. Madras Agric. J 2007;94: 89-96.
  • [29] Viegas-Crespo AM, Lopes PA, Pinheiro MT, Santos MC, Rodrigues PD, Nunes AC, Marques C, Mathias ML.Hepatic elemental contents and antioxidant enzyme activities in Algerian mice (Mus spretus) inhabiting a mine area in central Portugal.Sci. Total Environ 2003; 311: 101–109.
  • [30] Schleich CE, Beltrame MO, Carlos DA. Heavy metals accumulation in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae) from areas with different risk of contamination'. Folia Zool 2010; 2:108-114.
  • [31] Lourenço J, Pereira R, Gonçalves F, Mendo S. Metal bioaccumulation, genotoxicity and gene expression in the European wood mouse (Apodemus sylvaticus) inhabiting an abandoned uranium mining area. Sci. Total Environ 2013; 443:673–680.
  • [32] Arslan A, Kryštufek B, Matur F, Zima J. Review of chromosome races in blind mole rats (Spalax and Nannospalax). Folia Zool 2016; 4:249-301.
  • [33] Yağcı T. C- and NOR-banding karyotype analysis of Nannospalax xanthodon (2n=52, 2n=60) and new locality for 2n=52 cytotype from western Anatolia. Caryologia 2017; 71:7-12.
  • [34] SETAC-Society of Environmental Toxicology and Chemistry. Environmental contaminants in wildlife: interpreting tissue concentrations, in: W.N. Beyer, G.H. Heinz, A.W. Redmon-Norwood (Eds.), CRC Lewis, Boca Raton, 1996, 494 pp.
  • [35] Freedman B. Toxic elements, in: B. Freedman (Ed.), Environmental Ecology: The Ecological Effects of Pollution, Disturbance, and Other Stresses, Academic Press, London, 1995, pp. 62-93.
  • [36] Silva J, TRO Freitas, Heuser V, Marinho JR, Bittencourt F, Tadeu C, Cerski S, Kliemann LM, Erdtmann B. Effects of chronic exposure to coal in wild rodents (Ctenomys torquatus) evaluated by multiple methods and tissues. Mutation Research 2000; 470:39-51.
  • [37] Smith GJ, Rongstad OJ. Small mammal heavy metal concentrations from mined and control sites. Environ Pollut 1982; 28:121-134.
  • [38] Pankakoski E, Koivisto I, Hyvarinen H, Terhivuo J. Shrews as indicators of heavy metal pollution. Carnegie Museum Nat Hist Spec Publ. 1994; 18, 137–149.
  • [39] Komarnicki GJK. Tissue, sex and age specific accumulation of heavy metals (Zn, Cu, Pb, Cd) by populations of the mole (Talpa europaea L.) in a central urban area. Chemosphere 2000; 41:1593–1602.
  • [40] Lopes PA, Viegas-Crespo AM, Nunes AC, Pinheiro T, Marques C, Santos MA, Mathias ML. Influence of age, sex, and sexual activity on trace element levels and antioxidant enzyme activities in field mice (Apodemus sylvaticus and Mus spretus). Biol Trace Elem Res 2002; 85:227-239.
  • [41] Singh P, Sankhla V. In situ protective effect of curcumin on cadmium chloride induced genotoxicity in bone marrow chromosomes of Swiss albino mice. J Cell Mol Biol 2010; 2: 57-64.
  • [42] Jihen EH, Imed M, Fatima H, Abdelhamid K. Protective effects of selenium (Se) and zinc (Zn) on cadmium (Cd) toxicity in the liver of the rat: effects on the oxidative stress. Ecotoxicol Environ Saf 2009; 5:1559-1564.
  • [43] Jemai H, Lachkar HA, Messaoudi I, Kerkeni A. Effect of zinc pre-treatment on blood glutathione, serum zinc and kidney histological organization in male rats exposed to cadmium. J Trace Elem Med Bıo 2010; 4:277-288.
  • [44] Nevo E. Stress, adaptation, and speciation in the evolution of the blind mole rat, Spalax, in Israel. Mol. Phylogenetics Evol 2013; 66:515–525.
  • [45] Savic I, Nevo E.The Spalacidae; Evolutionary history, speciation and population biology, in; Evolution of Subterranean Mammals at the Organismal and Molecular Levels. Alan R. Liss New York: pp.129-153.
  • [46] Nevo E, Filippucci MG, Redi C, Korol A, Beiles A. Chromosomal speciation and adaptive radiation of mole rats in Asia Minor correlated with increased ecological stress. Proc Natl Acad Sci 1994b; 91: 8160-8164.
  • [47] Nevo E, Filippucci MG, Redi C, Simson S, Heth G, Beiles A. Karyotype and genetic evolution in speciation of subterranean mole rats of the genus Spalax in Turkey. Biol J Linn Soc 1995; 54: 203-229.
Toplam 46 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Yapısal Biyoloji , Ekoloji
Bölüm Makaleler
Yazarlar

Tuba Yağcı 0000-0003-1705-5107

Rafig Gurbanov 0000-0002-5293-6447

Yayımlanma Tarihi 30 Temmuz 2020
Yayımlandığı Sayı Yıl 2020 Cilt: 9 Sayı: 2

Kaynak Göster

APA Yağcı, T., & Gurbanov, R. (2020). HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, 9(2), 169-178. https://doi.org/10.18036/estubtdc.653015
AMA Yağcı T, Gurbanov R. HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS. Estuscience - Life. Temmuz 2020;9(2):169-178. doi:10.18036/estubtdc.653015
Chicago Yağcı, Tuba, ve Rafig Gurbanov. “HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS”. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 9, sy. 2 (Temmuz 2020): 169-78. https://doi.org/10.18036/estubtdc.653015.
EndNote Yağcı T, Gurbanov R (01 Temmuz 2020) HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 9 2 169–178.
IEEE T. Yağcı ve R. Gurbanov, “HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS”, Estuscience - Life, c. 9, sy. 2, ss. 169–178, 2020, doi: 10.18036/estubtdc.653015.
ISNAD Yağcı, Tuba - Gurbanov, Rafig. “HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS”. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 9/2 (Temmuz 2020), 169-178. https://doi.org/10.18036/estubtdc.653015.
JAMA Yağcı T, Gurbanov R. HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS. Estuscience - Life. 2020;9:169–178.
MLA Yağcı, Tuba ve Rafig Gurbanov. “HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS”. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, c. 9, sy. 2, 2020, ss. 169-78, doi:10.18036/estubtdc.653015.
Vancouver Yağcı T, Gurbanov R. HEAVY METAL-ASSOCIATED CHROMOSOMAL ABERRATIONS IN SUBTERRANEAN MAMMALS (RODENTIA: SPALACIDAE) FROM POLLUTED SOILS. Estuscience - Life. 2020;9(2):169-78.