Abstract
The Caspian region and specifically the Apsheron peninsula of Azerbaijan are known to be polluted with a variety of environmental contaminants. These complex mixtures of contaminants make risk assessment difficult. We used the flow cytometry method (FCM) and the micronucleus assay (MN) to assess chromosomal damage in aquatic turtles (Emys orbicularis, the European pond turtle; and Mauremys caspica, the Caspian turtle) inhabiting contaminated wetlands in Azerbaijan. Evidence of genetic damage was found for two sites, Neftchala and Sumgayit, relative to a reference site, Ali Bairamly. Sediment samples from each site were analyzed for PAHs and mercury to evaluate potential contaminant associations with genetic damage. A significant positive correlation was documented between three-ring PAH sediment concentrations and FCM estimates of chromosomal damage in E. orbicularis. These data combine to show that the contaminated wetlands in Sumgayit and Neftchala are genotoxic and that three-ring PAHs are likely a significant influence on observed genotoxicity.
Similar content being viewed by others
References
Alsabti K., Metcalfe C.D., (1995). Fish micronuclei for assessing genotoxicity in water Mutat. Res./Genet. Toxicol. 343:121–35
Amorim M.I.M., Mergler D., Bahia M.O., Dubeau H., Miranda D., Lebel J., Burbano R.R., Lucotte M., (2000). Cytogenetic damage related to low levels of methyl mercury contamination in the Brazilian Amazon Anais da Academia Brasileira de Ciencias 72:497–507
Andruchow J.E. (2003). Cancer incidence and mortality in the industrial city of Sumgayit, Azerbaijan: a descriptive study. M.S. Thesis, University of Alberta
Ayllon F., Garcia-Vazquez E.G., (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./Genet. Toxicol. Environ. Mutagen. 467:177–86
Betti C., Davini T., Barale R., (1992). Genotoxic activity of methyl mercury-chloride and dimethyl mercury in human-lymphocytes Mutat. Res. 281:255–60
Bickham J.W., Hanks B.G., Smolen M.J., Lamb T., Gibbons J.W., (1988). Flow cytometric analysis of the effects of low-level radiation exposure on natural populations of slider turtles (Pseudemys scripta) Arch. Environ. Contam. Toxicol. 17:837–41
Bickham J.W., Matson C.W., Islamzadeh A., Rowe G.T., Donnelly K.C., Swartz C.D., Rogers W.J., Wickliffe J.K., Autenrieth R.L., McDonald T.J., Politov D., Palatnikov G., Mekhtiev A.A., Kasimov R., (2003). Editorial: the unknown environmental tragedy in Sumgayit, Azerbaijan Ecotoxicology 12:507–10
Bickham J.W., Mazet J.A., Blake J., Smolen M.J., Lou Y., Ballachey B.E., (1998a). Flow-cytometric determination of genotoxic effects of exposure to petroleum in mink and sea otters Ecotoxicology 7:191–9
Bickham J.W., Rowe G.T., Palatnikov G., Mekhtiev A.A., Mekhtiev M., Kasimov R.Y., Hauschultz D.W., Wickliffe J.K., Rogers W.J., (1998b). Acute and genotoxic effects of Baku Harbor sediment on Russian sturgeon, Acipenser guildensteidti Bull. Environ. Contam. Toxicol. 61:512–8
Bickham J.W., Sawin V.L., Burton D.W., McBee K., (1992). Flow cytometric analysis of the effects of triethylenemelamine on somatic and testicular tissues of the rat Cytometry 13:368–73
Bickham J.W., Sawin V.L., McBee K., Smolen M.J., Derr J.N., (1994). Further flow cytometric studies of the effects of triethylenemelamine on somatic and testicular tissues of the rat Cytometry 15:222–9
Bombail V., Aw D., Gordon E., Batty J., (2001). Application of the comet and micronucleus assays to butterfish (Pholis gunnellus) erythrocytes from the Firth of Forth, Scotland Chemosphere 44:383–92
Bresler V., Bissinger V., Abelson A., Dizer H., Sturm A., Kratke R., Fishelson L., Hansen P.D., (1999). Marine molluscs and fish as biomarkers of pollution stress in littoral regions of the Red Sea, Mediterranean Sea and North Sea Helgoland Mar. Res. 53:219–43
Buchman M.F. (1999). NOAA Screening Quick Reference Tables, NOAA HAZMAT Report 99-1. Coastal Protection and Restoration Division, National Oceanic and Atmospheric Administration
Chen J.W., Peijnenburg W.J.G.M., Quan X., Chen S., Martens D., Schramm K.W., Kettrup A., (2001). Is it possible to develop a QSPR model for direct photolysis half-lives of PAHs under irradiation of sunlight? Environ. Pollut. 114:137–43
Chuang J.C., Wise S.A., Cao S., Mumford J.L., (1992). Chemical characterization of mutagenic fractions of particles from indoor coal combustion: a study of lung cancer in Xuan Wei, China Environ. Sci. Technol. 26:999–1004
Cicchetti R., Bari M., Argentin G., (1999). Induction of micronuclei in bone marrow by two pesticides and their differentiation with CREST staining: an in vivo study in mice Mutat. Res./Genet. Toxicol. Environ. Mutagen. 439:239–48
Cizmas L., Barhoumi R., Burghardt R.C., Reeves W.R., He L.Y., McDonald T.J., Donnelly K.C., (2003). A comparison of two methods for fractionating complex mixtures in preparation for toxicity analysis J. Toxicol. Environ. Health, Part A 66:1351–70
Cullen R. (1999). The rise and fall of the Caspian Sea. Natl. Geogr. 195:2–35
Custer T.W., Bickham J.W., Lyne T.B., Lewis T., Ruedas L.A., Custer C.M., Melancon M.J., (1994). Flow cytometry for monitoring contaminant exposure in black-crowned night-herons Arch. Environ. Contam. Toxicol. 27:176–9
Custer T.W., Custer C.M., Hines R.K., Sparks D.W., Melancon M.J., Hoffman D.J., Bickham J.W., Wickliffe J.K., (2000). Mixed-function oxygenases, oxidative stress, and chromosomal damage measured in lesser scaup wintering on the Indiana Harbor Canal Arch. Environ. Contam. Toxicol. 38:522–9
Dallas C.E., Evans D.L., (1990). Flow cytometry in toxicity analysis Nature 345:557–8
De Flora S., Bennicelli C., Bagnasco M., (1994). Genotoxicity of mercury compounds – a review Mutat. Res. 317:57–79
Dopp E., Saedler J., Stopper H., Weiss D.G., Schiffmann D., (1995). Mitotic disturbances and micronucleus induction in Syrian hamster embryo fibroblast cells caused by asbestos fibers Environ. Health Perspect. 103:268–71
Dopp E., Schiffmann D., (1998). Analysis of chromosomal alterations induced by asbestos and ceramic fibers Toxicol. Lett. 96–97:155–62
Dumont H., (1995). Ecocide in the Caspian Sea Nature 377:673–4
Ernst, C.H. and Barbour, R.W. (1989). Turtles of the World. Smithsonian Institution Press, Washington D.C
Gauthier J.M., Dubeau H., Rassart E., (1999). Induction of micronuclei in vitro by organochlorine compounds in beluga whale skin fibroblasts Mutat. Res./Genet. Toxicol. Environ. Mutagen. 439:87–95
George L.S., Dallas C.E., Brisbin I.L.J., Evans D.L., (1991). Flow cytometric DNA analysis of ducks accumulating 137Cs on a reactor reservoir Ecotoxicol. Environ. Safety 21:337–47
Heitkamp M.A., Cerniglia C.E., (1987). Effects of chemical-structure and exposure on the microbial-degradation of polycylic aromatic-hydrocarbons in fresh-water and estuarine ecosystems Environ. Toxicol. Chem. 6:535–46
Izquierdo J.I., Machado G., Ayllon F., d’Amico V.L., Bala L.O., Vallarino E., Elias R., Garcia-Vazquez E., (2003). Assessing pollution in coastal ecosystems: a preliminary survey using the micronucleus test in mussel Mytilus edulis Ecotoxicol. Environ. Safety 55:24–9
Jaurand M.-C., (1997). Mechanisms of fiber-induced genotoxicity Environ. Health Perspect. 105:1073–84
Jenkins J.R., (1996). Diagnostics and clinical techniques In Mader D.R., (Ed.) Reptile Medicine and Surgery Philadelphia: W.B. Saunders Company pp. 264–76
Kajiwara N., Niimi S., Watanabe M., Ito Y., Takahashi S., Tanabe S., Khuraskin L.S., Miyazaki N., (2002). Organochlorine and organotin compounds in Caspian seals (Phoca caspica) collected during an unusual mortality event in the Caspian Sea in 2000 Environ. Pollut. 117:391–402
Kajiwara N., Ueno D., Monirith I., Tanabe S., Pourkazemi M., Aubrey D.G., (2003). Contamination by organochlorine compounds in sturgeons from Caspian Sea during 2001 and 2002 Marine Pollut. Bull. 46:741–7
Kocan R.M., Matta M.B., Salazar S.M., (1996). Toxicity of weathered coal tar for shortnose sturgeon (Acipenser brevirostrum) embryos and larvae Arch. Environ. Contam. Toxicol. 31:161–5
Kovalkovicova N., Kacmar P., Sutiakova I., Sulik E., Mikula I., Pistl J., Mlynarcikova H., Legath J., (2000). Assessment of the ability of endosulfan to induce micronuclei in vitro in cultured sheep lymphocytes J. Trace Microprobe Techniq. 18:221–6
Lamb T., Bickham J.W., Gibbons J.W., Smolen M.J., McDowell S., (1991). Genetic damage in a population of slider turtles (Trachemys scripta) inhabiting a radioactive reservoir Arch. Environ. Contam. Toxicol. 20:138–42
Lamb T., Bickham J.W., Lyne T.B., Gibbons J.W., (1995). The slider turtle as an environmental sentinel: multiple tissue assays using flow cytometric analysis Ecotoxicology 4:5–13
Lingenfelser S.K., Dallas C.E., Jagoe C.H., Chesser R.K., Smith M.H., Lomakin M., (1997a). Variation in blood cell DNA in Carassius carassius from ponds near Chernobyl, Ukraine Ecotoxicology 6:187–203
Lingenfelser S.K., Dallas C.E., Jagoe C.H., Smith M.H., Brisbin I.L.J., Chesser R.K., (1997b). Variation in DNA content of blood cells of largemouth bass from contaminated and uncontaminated waters Environ. Toxicol. Chem. 16:2136–43
Lowcock L.A., Sharbel T.F., Bonin J., Ouellet M., Rodrigue J., Des Granges J.-L., (1997). Flow cytometric assay for in vivo genotoxic effects of pesticides in green frogs (Rana clamitans) Aquat. Toxicol. 38:241–55
Lyne T.B., Bickham J.W., Lamb T., Gibbons J.W., (1992). The application of bioassays in risk assessment of environmental-pollution Risk Analysis 12:361–5
Matson, C.W., Franson, J.C., Hollmén, T., Kilpi, M., Hario, M., Flint, P.L. and Bickham, J.W., (2004). Evidence of chromosomal damage in Common Eiders (Somateria mollissima) from the Baltic Sea. Marine Pollut. Bull. 49:1066–1071
Matsumoto Y., Sakai S., Kato T., Nakajima T., Satoh H., (1998). Long-term trends of particulate mutagenic activity in the atmosphere of Sapporo 1. Determination of mutagenic activity by the conventional tester strains TA98 and TA100 during an 18-year period (1974–1992) Environ. Sci. Technol. 32:2665–71
McBee K., Bickham J.W., (1988). Petrochemical-related DNA damage in wild rodents detected by flow cytometry Bull. Environ. Contam. Toxicol. 40:343–9
Mill T., Mabey W.R., Lan B.Y., Baraze A., (1981). Photolysis of polycyclic aromatic hydrocarbons in water Chemosphere 10:1281–90
Mills M.A., Bonner J.S., McDonald T.J., Page C.A., Autenrieth R.L., (2003). Intrinsic bioremediation of a petroleum-impacted wetland Marine Pollut. Bull. 46:887–99
Misra R.K., Easton M.D.L., (1999). Comment on analyzing flow cytometric data for comparison of mean values of the coefficient of variation of the G1 peak Cytometry 36:112–6
Nepomuceno J.C., Ferrari I., Spano M.A., Centeno A.J., (1997). Detection of micronuclei in peripheral erythrocytes of Cyprinus carpio exposed to metallic mercury Environ. Mol. Mutagen. 30:293–7
Ochi T., (2002). Methylmercury, but not inorganic mercury, causes abnormality of centrosome integrity (multiple foci of gamma-tubulin), multipolar spindles and multinucleated cells without microtubule disruption in cultured Chinese hamster V79 cells Toxicology 175:111–21
Ogura H., Takeuchi T., Morimoto K., (1996). A comparison of the 8-hydroxydeoxyguanosine, chromosome aberrations and micronucleus techniques for the assessment of the genotoxicity of mercury compounds in human blood lymphocytes Mutat. Res./Rev. Genet. Toxicol. 340:175–82
Queiroz M.L.S., Bincoletto C., Quadros M.R., De Capitani E.M., (1999). Presence of micronuclei in lymphocytes of mercury exposed workers Immunopharmacol. Immunotoxicol. 21:141–50
Reeves W.R., Barhoumi R., Burghardt R.C., Lemke S.L., Mayura K., McDonald T.J., Phillips T.D., Donnelly K.C., (2001). Evaluation of methods for predicting the toxicity of polycyclic aromatic hydrocarbon mixtures Environ. Sci. Technol. 35:1630–36
Sanchez-Galan S., Linde A.R., Ayllon F., Garcia-Vazquez E., (2001). Induction of micronuclei in eel (Anguilla anguilla L.) by heavy metals Ecotoxicol. Environ. Safety 49:139–43
Sanchez-Galan S., Linde A.R., Garcia-Vazquez E., (1999). Brown trout and European minnow as target species for genotoxicity tests: differential sensitivity to heavy metals Ecotoxicol. Environ. Safety 43:301–304
Schantz M.M., Nichols J.J., Wise S.A., (1997). Evaluation of pressurized fluid extraction for the extraction of environmental matrix reference materials Anal. Chem. 69:4210–19
Schreiner C.A., (2003). Genetic toxicity of naphthalene: a review J. Toxicol. Environ. Health, Part B, Crit. Rev. 6:161–83
Shelton N., (2003). Azerbaijan: environmental conditions and outlook Ambio 32:302–306
Swartz C.D., Donnelly K.C., Islamzadeh A., Rowe G.T., Rogers W.J., Palatnikov G., Mekhtiev A.A., Kasimov R., McDonald T.J., Wickliffe J.K., Bickham J.W., (2003). Chemical contaminants and their effects in fish and wildlife from the industrial zone of Sumgayit, Republic of Azerbaijan Ecotoxicology 12:511–23
Tanabe S., Niimi S., Minh T.B., Miyazaki N., Petrov E.A., (2003). Temporal trends of persistent organochlorine contamination in Russia: a case study of Baikal and Caspian Seal Arch. Environ. Contam. Toxicol. 44:533–45
Theodorakis C.W., Bickham J.W., Lamb T., Medica P.A., Lyne T.B., (2001). Integration of genotoxicity and population genetic analyses in kangaroo rats (Dipodomys merriami) exposed to radionuclide contamination at the Nevada test site, USA Environ. Toxicol. Chem. 20:317–26
Thies M.L., Thies K., McBee K., (1996). Organochlorine pesticide accumulation and genotoxicity in Mexican free-tailed bats from Oklahoma and New Mexico Arch. Environ. Contam. Toxicol. 30:178–87
U.S. Environmental Protection Agency. (2000). Method 7473, Mercury in solids and solutions by thermal decomposition, amalgamation, and atomic absorption spectrometry. Test Methods for Evaluating Solid Waste, Physical/Chemical Methods, SW-846, Update IVA, pp. Washington, DC: U.S. Government Printing Office
Vindelov L.L., Christiansen I.J., (1994). Detergent and proteolytic enzyme-based techniques for nuclear isolation and DNA content analysis In Darzynkiewicz Z., Robinson J.P., Crissman H.A., (Eds) Flow Cytometry: Methods in Cell Biology 2 Part A New York: Academic Press pp. 219–29
Watanabe M., Tanabe S., Tatsukawa R., Amano M., Miyazaki N., Petrov E.A., Khuraskin S.L., (1999). Contamination levels and specific accumulation of persistent organochlorines in Caspian seal (Phoca caspica) from the Caspian sea, Russia Arch. Environ. Contam. Toxicol. 37:396–407
Acknowledgments
Funding was provided by the National Institutes of Environmental Health Sciences Grant ES04917. We thank the Sumgayit Centre for Environmental Rehabilitation and Arif A. Mekhtiev and Rafik Kasimov of the Karaev Institute of Physiology, Academy of Sciences of the Azerbaijan Republic for logistical and field support. We also thank Dmitri Politov and William J. Rogers for assistance in field collections.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
MATSON, C.W., PALATNIKOV, G., ISLAMZADEH, A. et al. Chromosomal Damage in Two Species of Aquatic Turtles (Emys orbicularis and Mauremys caspica) Inhabiting Contaminated Sites in Azerbaijan. Ecotoxicology 14, 513–525 (2005). https://doi.org/10.1007/s10646-005-0001-0
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-005-0001-0