Assessment of genotoxicity and depuration of anthracene in the juvenile coastal fish Trachinotus carolinus using the comet assay

Hasue, Fabio Matsu; Passos, Maria José de Arruda Campos Rocha; Santos, Thaís da Cruz Alves dos; Rocha, Arthur José da Silva; Vignardi, Caroline Patrício; Sartorio, Priscila Verônica; Gomes, Vicente; Ngan, Phan Van

Abstracts

In the environment, anthracene is characterized as being persistent, bioaccumulative and toxic to aquatic organisms. Biotransformation of xenobiotic substances, such as anthracene, produces reactive oxygen species that may induce DNA strand breaks. The aim of the present study was to evaluate the DNA damage in juvenile T. carolinus exposed to different concentrations (8, 16 and 32 µg.L-1) of anthracene for 24 h in the dark then subsequently allowed to depurate in clean water for different periods of time (48, 96 or 144 h) using the comet assay. Our results show that anthracene is genotoxic to T. carolinus and that DNA damage was dose- and depuration/time- dependent. Anthracenegenotoxicity was observed in all experimental concentrations. Depuration seemed to be more efficient in fish exposed to thelowest anthracene concentration and maintained in clean water for 96 h.

Polycyclic aromatic hydrocarbons (PAH); Anthracene; DNA damage; Reactive oxygen species (ROS); Marine fish

Ambientalmente, o antraceno é considerado persistente, bioacumulativo e tóxico para organismos aquáticos. A biotransformação de substâncias xenobióticas, como o antraceno, produz espécies reativas de oxigênio que podem agir sobre o DNA. O objetivo deste trabalho foi avaliar o dano ao DNA em T. carolinus expostos a diferentes concentrações de antraceno (8, 16 e 32 µg.L-1) por 24 h no escuro e subsequentemente mantidos em água limpa para depuração por três diferentes períodos de tempo (48, 96 e 144 h) através de ensaio cometa. Os resultados obtidos demonstram que o antraceno é genotóxico para T. carolinus e o dano ao DNA foi dose- e tempo de depuração- dependente. A genotoxicidade do antraceno foi detectada nas três concentrações utilizadas. A depuração pareceu ser mais eficiente nos peixes expostos a menor concentração de antraceno e mantidos por 96 h em água limpa.

Hidrocarbonetos policíclicos aromáticos (HPA); Antraceno; Dano ao DNA; Espécies reativas de oxgênio (EROS); Peixe marinho

References

AKCHA, F.; HUBERT, F. V.; PFHOL-LESZKOWICZ, A. Potential value of the comet assay and DNA adduct measurement in dab (Limanda limanda) for assessment of in situ exposure to genotoxic compounds. Mutat.Res., v. 534, n. 1/2, p. 21-32, 2003.
AL-SABTI, K.; METCALFE, C. D. Fish micronuclei for assessing genotoxicity in water.Mutat.Res., v. 343, n. 2/3, p. 121-135, 1995.
AMADO, L. L.; ROSA, C. E.; LEITE, A. M.; MORAES, L.; PIRES, W. V.; PINHO, G. L. L.; MARTINS, C. M. G.; ROBALDO, R. B.; NERY, L. E. M.; MONSERRAT, J. M.; BIANCHINI, A.; MARTINEZ, P. E.; GERACITANO, L. A. Biomarkers in croakers Micropogonias furnieri (Teleostei: Sciaenidae) from polluted and non-polluted areas from the Patos Lagoon estuary (Southern Brazil): evidences of genotoxic and immunological effects. Mar. Pollut. Bull., v. 52, n. 2, p. 199-206, 2006.
BEDDING, N. D.; MCINTYRE, A. E.; PERRY, R.; LESTER, J. N. Organic contaminants in the aquatic environment. II. Behavior and fate in hydrological cycle. Sci. Total Environ., v. 26, p. 255-312, 1983.
BÍCEGO, M. C.; TANIGUCHI, S.; YOGUI, G. T.; MONTONE, R. C.; MOREIRA DA SILVA, D. A.; LOURENÇO, R. A.; CASTRO MARTINS, C.; SASAKI, S. T.; PELLIZARI, V. H.; WEBER, R. R. Assessment of contamination by polychlorinated biphenyls and aliphatic and aromatic hydrocarbons in sediments of the Santos and São Vicente Estuary System, São Paulo, Brazil. Mar. Pollut. Bull., v. 56, n. 12, p. 1804-1816, 2006.
BOWLING, J. W.; LEVERSEE, G. J.; LANDRUM, P. F.; GIESY, J. P. Acute mortality of anthracene-contaminated fish exposed to sunlight. Aquat.Toxicol., v. 3, n. 1, p. 79-90, 1983.
CHIZHOVA, T.; HAYAKAWA, K.; TISHCHENKO, P.; NAKASE, H.; KOUDRYASHOVA, YU. Distribution of PAHs in the northwestern part of the Japan Sea. Deep Sea Res., Part II,v. 86/87, pt. II, p. 19-24, 2013.
CHOI, J.; ORIS, J. T. Assessment of the toxicity of anthracene photo-modification products using the topminnow (Poeciliopsis lucida) hepatomacell line (PLHC-1). Aquat.Toxicol., v. 65, n.3, p. 243-251, 2003.
COLLINS, A. R. The Comet assay damage for DNA and repair: principles, applications, and limitations. Mol. Biotechnol., v. 26, n. 3, p. 249-261, 2004.
COTELLE, S.; FÉRARD, J. F. Comet assay in genetic ecotoxicology: a review. Environ. Mol. Mutagen., v. 34, n. 4, p. 246-255, 1999.
CRABTREE, R. E.; HOOD, P. B.; SNODGRASS, D. Age, growth and reproduction of permit (Trachinotus falcatus) in Florida waters. Fish.Bull., v. 100, n. 1, p. 26-34, 2002.
DI GIULIO, R. T.; BENSON, W. H.; SANDERS, B. M.; VAN VELD, P. A. Biochemical mechanisms metabolism, adaptation and toxicity. In: RAND, G. M. (Ed.). Fundamentals of aquatic toxicology: effects, environmental fate, and risk assessment 2.ed. Washington: Taylor & Francis, 1995. p. 523-561.
EUROPEAN CHEMICAL AGENCY. Support Document for Identification of Anthracene as a Substance of Very High Concern, 2008. 21 p. Available at: http://echa.europa.eu/documents/10162/13638/svhc_supdoc_anthracene_publication_en.pdf Accessed in: 14 mar. 2010.
FRENZILLI, G.; NIGRO, A.; LYONS, B. P.The comet assay for the evaluation of genotoxic impact in aquatic environments. Mutat.Res., v. 681, n.1, p. 80-92, 2009.[Review]
GARCÍA, O.; MANDINA, T.; LAMADRID, A. I.; DIAZ, A.; REMIGIO, A.; GONZALEZ, Y.; PILOTO, J.; GONZALEZ, J. E.; ALVAREZ, A. Sensitivity and variability of visual scoring in the comet assay: results of an inter-laboratory scoring exercise with the use of silver staining. Mutat. Res., v. 556, n. 1/2, p. 25-34, 2004.
GOMES, V.; PASSOS, M. J. A. C. R.; LEME, N. M. P.; SANTOS,T. C. A.; CAMPOS, D. Y. F.; HASUE, F. M.;PHAN, V. N. Photo-induced toxicity of anthracene in the Antarctic shallow water amphipod Gondogeneia antarctica Polar Biol., v. 32, n. 7, p. 1009-1021, 2009.
GOMES, V.; PASSOS, M. J. A. C. R.; SANTOS, T. C. A.; CAMPOS, D. Y. F.; USSAMI, K. A.; HASUE, F. M.; PHAN, V. N.DNA strand breaks in caged Antarctic coastal fishes (Trematomus newnesi), following exposure to the waters in front of the Brazilian Antarctic Research Station "Comandante Ferraz", King George Island. Pesqui. Antart. Bras., v. 5 p. 61-70, 2012.
GONTIJO, A. M. M. C.; TICE, R. Teste do cometa para a detecção de dano no DNA e reparo em células individualizadas. In: RIBEIRO, L. R.; SALVADORI, D. M. F.; MARQUES, E. K. (Orgs.). Mutagênese ambiental Canoas: Ulbra, 2003. p. 247-279.
GROFF, A. A.; SILVA, J.; NUNES, E.A.; IANISTCKI, M.; GUECHEVA, T. N.; OLIVEIRA, A. M.; OLIVEIRA, C. P. F.; VAL, A. L.; HENRIQUES, J. A. P.UVA/UVB-induced genotoxicity and lesion repair in Colossoma macropomum and Arapaima gigas Amazonian fish. J. Photochem. Photobiol., B, v. 99, n. 2, p. 93-99, 2010.
HASEGAWA, M.; SUZUKI, A.; MATSUMURA, S.; TOSHIMA, K. Molecular design, chemical synthesis, and evaluation of novel anthracene derivatives as a new family of protein photocleavers. Sci. Technol. Adv. Mater., v. 7, n. 2, p. 169-174, 2006.
HATCH, A. C.; BURTON Jr., G. A. Photo-induced toxicity of PAHs to Hyalella azteca and Chironomus tentans: effects of mixtures and behavior. Environ. Pollut., v. 106, n.2, p. 157-167, 1999.
JORY, D. E.; IVERSEN, E. S.; LEWIS, R. H. Culture of the fishes of the genus Trachinotus (Carangidae) in the western Atlantic: prospects and problems. J.World Maric. Soc., v. 16, n. 1/4, p. 87-94, 1985.
KANGAN, J.; KAGAN, E. D.; KAGAN, I. A.; KAGAN, P. A.; QUIGLEY, S. The phototoxicity of non-carcinogenic polycyclic aromatic hydrocarbons in aquatic organisms. Chemosphere, v. 14, n. 11/12, p. 1829-1834, 1985.
KIENE, R. P.; CAPONE, D. G. Effects of organic pollutants on methanogenesis, sulfate reduction and carbon dioxide evolution in salt marsh sediments. Mar. Environ. Res., v. 13, p. 141-160, 1984.
LAW, R. J.; DAWES, V. J.; WOODHEAD, R. J.; MATTHIESSEN, P. Polycyclic Aromatic Hydrocarbons (PAH) in seawater around England and Wales. Mar. Pollut. Bull., v. 34, n. 5, p. 306-322, 1997.
LEE, R. F.; PAGE, D. S. Petroleum hydrocarbons and their effects in subtidal regions after major oil spills. Mar. Pollut. Bull., v. 34, n. 11, p. 928-940, 1997.
LEE, R. F.; STEINERT, S. Use of the singles cell electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat. Res., v. 544, n. 1, p. 43-64, 2003.
MALLAKIN, A.; DIXON, D. G.; GREENBERG, B. M. Pathway of anthracene modification under simulated solar radiation. Chemosphere, v. 40, n. 12, p. 1435-1441, 2000.
MASKAOUI, K.; ZHOU, J. L.; HONG, H. S.; ZHANG, Z. L. Contamination by polycyclic aromatic hydrocarbons in the Jiulong River Estuary and Western Xiamen Sea, China. Environ. Pollut., v. 118, n.1, p. 109-122, 2002.
MCELROY, A. E.; FARRINGTON, J. W.; TEAL, J. M. Bioavailability of polycyclic aromatic hydrocarbons in the aquatic environment. In: VARANASI, U. (Ed.) Metabolism of polycyclic aromatic hydrocarbons in the aquatic environment Boca Raton: CRC Press, 1989. p. 1-39.
MEDEIROS, P. M.; BÍCEGO, M. C. Investigation of natural and anthropogenic hydrocarbon inputs in sediment using geochemical markers. II. São Sebastião, SP-Brazil. Mar. Pollut. Bull., v. 49, n. 11-12, p. 892-899, 2004.
MEDEIROS, P. M.; BÍCEGO, M. C.; CASTELÃO, R. M.; DEL ROSSO, C.; FILMANN, G.; ZAMBONI, A. J. Natural and anthropogenic hydrocarbon inputs to sediments of Patos Lagoon Estuary, Brazil. Environ. Int., v. 31, n. 1, p. 77-87, 2005.
MENEZES, N. A.; FIGUEIREDO, J. L. Manual de peixes marinhos do sudeste do Brasil. IV. Teleostei 3 São Paulo: Museu de Zoologia da Universidade de São Paulo, 1980. 96 p.
MOHANTY, G.; MOHANTY, J.; NAYAK, A. K.; MOHANTY, S.; DUTTA, S. K. Application of comet assay in the study of DNA damage and recovery in rohu (Labeo rohita) fingerlings after an exposure to phorate, an organophosphate pesticide. Ecotoxicology, v. 20, n. 1, p. 283-292, 2011.
NEFF, J. M. Polycyclic aromatic hydrocarbons in the aquatic environment: sources, fates and biological effects. London: Applied Science Publishers, 1979. 262 p.
NIANG, T. M. S., PESSANHA, A. L. M.; ARAÚJO, F. G. Dieta de juvenis de Trachinotus carolinus (Actinopterygii, Carangidae) em praias arenosas na costa do Rio de Janeiro. Iheringia, Ser. Zool., v. 100, n. 1, p. 35-42, 2010.
ORIS, J. T.; GIESY Jr., J. P. The photoenhanced toxicity of anthracene to juvenile sunfish (Lepomis spp.). Aquat. Toxicol., v. 6, n. 2, p. 133-146, 1985.
ORIS, J. T.; GIESY Jr., J. P. The photo-induced toxicity of polycyclic aromatic hydrocarbons to larvae of the fathead minnow (Pimephales promelas). Chemosphere, v. 16, n. 7, p. 1395-1404, 1987.
PACHECO, M.; SANTOS, M. A. Biotransformation, genotoxic, and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicol. Environ. Saf., v. 53, n. 3, p. 331-347, 2002.
PELLETIER, E.; SARGIAN, P.; PAYET, J.; DEMERS, S. Ecotoxicological effects of combined UVB and organic contaminants in coastal waters: a review. Photochem. Photobiol., v. 82, n. 4, p. 981-993, 2006.
RAND, G. M. Fish toxicity studies. In: DI GIULIO, R. T.; HINTON, D. E. (Eds.). The toxicology of fishes Boca Raton: CRC Press, 2008. p. 659-681.
REN, H.; KAWAGOE, T.; JIA, H.; ENDO, H.; KITAZAWA, A.; GOTO, S.; HAYASHI, T. Continuous surface seawater surveillance on poly aromatic hydrocarbons (PAHs) and mutagenicity of East and South China Seas. Estuarine, Coastal Shelf Sci., v. 86, n. 3, p. 395-400, 2010.
ROCHA, A. J. S.; SANTOS, T. C.; GOMES, V.; BÍCEGO, M. C.; BARBOSA, A. C. R. A.; PASSOS, M. J. A. C. R.; HASUE, F. M.; PHAN, V. N. Assessment of trophic transfer of benzo(a)pyrenegenotoxicity from the post-larval pink shrimp F. brasiliensis to juvenile Florida pompano T. carolinus Environ. Toxicol. Pharmacol., v. 34, n. 3, p. 969-976, 2012.
SANTOS, T. C. A.; PHAN, V. N.; PASSOS, M. J. A. C. R.; GOMES, V. Effects of naphthalene on metabolic rate and ammonia excretion of juvenile Florida pompano, Trachinotus carolinus J. Exp. Mar. Biol. Ecol., v. 335, n. 1, p. 82-90, 2006.
SCHIRMER, K.; CHAN, A. G. J.; GREENBERG, B. M.; DIXON, D. G.; BOLS, N. C. Ability of 16 priority PAHs to be photocytotoxic to a cell line from the rainbow trout Gill. Toxicology, v. 127, p. 143-155, 1998.
SINGH, N. P.; MCCOY, M. T.; TICE, R. R.; SCHNEIDER; E. L.A simple technique for quantitation of low level of DNA damage in individual cells. Exp. Cell Res., v. 175, n. 1, p. 184-191, 1988.
TICE, R. R.; AGURELL, E.; ANDERSON, D.; BURLINSON, B.; HARTMANN, A.; KOBAYASHI, H.; MIYAMAE, Y.; ROJAS, E.; RYU, J. C.; SASAKI, Y. F. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ. Mol. Mutagen., v. 35, n. 3, p. 206-221, 2000.
TOSHIMA, K.; HASEGAWA, M.; SHIMIZU, J.; MATSUMURA, S. Molecular design, chemical synthesis and biological evaluation of anthracene-carbohydrate hybrids as novel DNA photocleaving and photoselective cytotoxic agents. ARKIVOC, v.2004, n.13, p. 28-35, 2004.
TOYOOKA, T.; IBUKI, Y.DNA damage induced by coexposure to PAHs and light. Environ. Toxicol. Pharmacol., v. 23, n. 2, p. 256-263, 2007.
ULUPINAR, M.; OKUMUS, I. Detection of mutagenic-carcinogenic pollutants in aquatic system using cytogenetic methods in fish. Turk. J. Zool., v. 26, p. 141-148, 2002.
UNITED STATES. Department of Health and Human Services. Public Health Services. Agency for Toxic Substances and Disease Registry. Toxicological profile for polycyclic aromatic hydrocarbons Atlanta: Agency for Toxic Substances and Disease Registry, 1995. 30 p.
VANZELLA, T. P.; MARTINEZ, C. B. R.; CÓLUS, I. M. S. Genotoxic and mutagenic effects of diesel oil water soluble fraction on a neotropical fish species. Mutat. Res., v. 631, n. 1, p. 36-43, 2007.
VIEIRA, L. R.; SOUSA, A.; FRASCO, M. F.; LIMA, I.; MORGADO, F.; GUILHERMINO, L. Acute effects of Benzo[a]pyrene, anthracene and a fuel oil on biomarkers of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Sci. Total Environ., v. 395, n. 2/3, p. 87-100, 2008.
VIGURI, J.; VERDE, J.; IRABIEN, A. Environmental assessment of polycyclic aromatic hydrocarbons (PAHs) in surface sediments of the Santander Bay, Northern Spain. Chemosphere, v. 48, n. 2, p. 157-165, 2002.
ZAR, J. H. Biostatistical analysis 3.ed. Upper Saddle River: Prentice-Hall, 1996. 918 p.

Publication Dates

Publication in this collection
10 Apr 2014
Date of issue
Dec 2013

History

Received
18 Oct 2012
Accepted
06 Dec 2013
Reviewed
28 Nov 2013

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] AKCHA, F.; HUBERT, F. V.; PFHOL-LESZKOWICZ, A. Potential value of the comet assay and DNA adduct measurement in dab (Limanda limanda) for assessment of in situ exposure to genotoxic compounds. Mutat.Res., v. 534, n. 1/2, p. 21-32, 2003.

[2] AL-SABTI, K.; METCALFE, C. D. Fish micronuclei for assessing genotoxicity in water.Mutat.Res., v. 343, n. 2/3, p. 121-135, 1995.

[3] AMADO, L. L.; ROSA, C. E.; LEITE, A. M.; MORAES, L.; PIRES, W. V.; PINHO, G. L. L.; MARTINS, C. M. G.; ROBALDO, R. B.; NERY, L. E. M.; MONSERRAT, J. M.; BIANCHINI, A.; MARTINEZ, P. E.; GERACITANO, L. A. Biomarkers in croakers Micropogonias furnieri (Teleostei: Sciaenidae) from polluted and non-polluted areas from the Patos Lagoon estuary (Southern Brazil): evidences of genotoxic and immunological effects. Mar. Pollut. Bull., v. 52, n. 2, p. 199-206, 2006.

[4] BEDDING, N. D.; MCINTYRE, A. E.; PERRY, R.; LESTER, J. N. Organic contaminants in the aquatic environment. II. Behavior and fate in hydrological cycle. Sci. Total Environ., v. 26, p. 255-312, 1983.

[5] BÍCEGO, M. C.; TANIGUCHI, S.; YOGUI, G. T.; MONTONE, R. C.; MOREIRA DA SILVA, D. A.; LOURENÇO, R. A.; CASTRO MARTINS, C.; SASAKI, S. T.; PELLIZARI, V. H.; WEBER, R. R. Assessment of contamination by polychlorinated biphenyls and aliphatic and aromatic hydrocarbons in sediments of the Santos and São Vicente Estuary System, São Paulo, Brazil. Mar. Pollut. Bull., v. 56, n. 12, p. 1804-1816, 2006.

[6] BOWLING, J. W.; LEVERSEE, G. J.; LANDRUM, P. F.; GIESY, J. P. Acute mortality of anthracene-contaminated fish exposed to sunlight. Aquat.Toxicol., v. 3, n. 1, p. 79-90, 1983.

[7] CHIZHOVA, T.; HAYAKAWA, K.; TISHCHENKO, P.; NAKASE, H.; KOUDRYASHOVA, YU. Distribution of PAHs in the northwestern part of the Japan Sea. Deep Sea Res., Part II,v. 86/87, pt. II, p. 19-24, 2013.

[8] CHOI, J.; ORIS, J. T. Assessment of the toxicity of anthracene photo-modification products using the topminnow (Poeciliopsis lucida) hepatomacell line (PLHC-1). Aquat.Toxicol., v. 65, n.3, p. 243-251, 2003.

[9] COLLINS, A. R. The Comet assay damage for DNA and repair: principles, applications, and limitations. Mol. Biotechnol., v. 26, n. 3, p. 249-261, 2004.

[10] COTELLE, S.; FÉRARD, J. F. Comet assay in genetic ecotoxicology: a review. Environ. Mol. Mutagen., v. 34, n. 4, p. 246-255, 1999.

[11] CRABTREE, R. E.; HOOD, P. B.; SNODGRASS, D. Age, growth and reproduction of permit (Trachinotus falcatus) in Florida waters. Fish.Bull., v. 100, n. 1, p. 26-34, 2002.

[12] DI GIULIO, R. T.; BENSON, W. H.; SANDERS, B. M.; VAN VELD, P. A. Biochemical mechanisms metabolism, adaptation and toxicity. In: RAND, G. M. (Ed.). Fundamentals of aquatic toxicology: effects, environmental fate, and risk assessment 2.ed. Washington: Taylor & Francis, 1995. p. 523-561.

[13] EUROPEAN CHEMICAL AGENCY. Support Document for Identification of Anthracene as a Substance of Very High Concern, 2008. 21 p. Available at: http://echa.europa.eu/documents/10162/13638/svhc_supdoc_anthracene_publication_en.pdf Accessed in: 14 mar. 2010.

[14] FRENZILLI, G.; NIGRO, A.; LYONS, B. P.The comet assay for the evaluation of genotoxic impact in aquatic environments. Mutat.Res., v. 681, n.1, p. 80-92, 2009.[Review]

[15] GARCÍA, O.; MANDINA, T.; LAMADRID, A. I.; DIAZ, A.; REMIGIO, A.; GONZALEZ, Y.; PILOTO, J.; GONZALEZ, J. E.; ALVAREZ, A. Sensitivity and variability of visual scoring in the comet assay: results of an inter-laboratory scoring exercise with the use of silver staining. Mutat. Res., v. 556, n. 1/2, p. 25-34, 2004.

[16] GOMES, V.; PASSOS, M. J. A. C. R.; LEME, N. M. P.; SANTOS,T. C. A.; CAMPOS, D. Y. F.; HASUE, F. M.;PHAN, V. N. Photo-induced toxicity of anthracene in the Antarctic shallow water amphipod Gondogeneia antarctica Polar Biol., v. 32, n. 7, p. 1009-1021, 2009.

[17] GOMES, V.; PASSOS, M. J. A. C. R.; SANTOS, T. C. A.; CAMPOS, D. Y. F.; USSAMI, K. A.; HASUE, F. M.; PHAN, V. N.DNA strand breaks in caged Antarctic coastal fishes (Trematomus newnesi), following exposure to the waters in front of the Brazilian Antarctic Research Station "Comandante Ferraz", King George Island. Pesqui. Antart. Bras., v. 5 p. 61-70, 2012.

[18] GONTIJO, A. M. M. C.; TICE, R. Teste do cometa para a detecção de dano no DNA e reparo em células individualizadas. In: RIBEIRO, L. R.; SALVADORI, D. M. F.; MARQUES, E. K. (Orgs.). Mutagênese ambiental Canoas: Ulbra, 2003. p. 247-279.

[19] GROFF, A. A.; SILVA, J.; NUNES, E.A.; IANISTCKI, M.; GUECHEVA, T. N.; OLIVEIRA, A. M.; OLIVEIRA, C. P. F.; VAL, A. L.; HENRIQUES, J. A. P.UVA/UVB-induced genotoxicity and lesion repair in Colossoma macropomum and Arapaima gigas Amazonian fish. J. Photochem. Photobiol., B, v. 99, n. 2, p. 93-99, 2010.

[20] HASEGAWA, M.; SUZUKI, A.; MATSUMURA, S.; TOSHIMA, K. Molecular design, chemical synthesis, and evaluation of novel anthracene derivatives as a new family of protein photocleavers. Sci. Technol. Adv. Mater., v. 7, n. 2, p. 169-174, 2006.

[21] HATCH, A. C.; BURTON Jr., G. A. Photo-induced toxicity of PAHs to Hyalella azteca and Chironomus tentans: effects of mixtures and behavior. Environ. Pollut., v. 106, n.2, p. 157-167, 1999.

[22] JORY, D. E.; IVERSEN, E. S.; LEWIS, R. H. Culture of the fishes of the genus Trachinotus (Carangidae) in the western Atlantic: prospects and problems. J.World Maric. Soc., v. 16, n. 1/4, p. 87-94, 1985.

[23] KANGAN, J.; KAGAN, E. D.; KAGAN, I. A.; KAGAN, P. A.; QUIGLEY, S. The phototoxicity of non-carcinogenic polycyclic aromatic hydrocarbons in aquatic organisms. Chemosphere, v. 14, n. 11/12, p. 1829-1834, 1985.

[24] KIENE, R. P.; CAPONE, D. G. Effects of organic pollutants on methanogenesis, sulfate reduction and carbon dioxide evolution in salt marsh sediments. Mar. Environ. Res., v. 13, p. 141-160, 1984.

[25] LAW, R. J.; DAWES, V. J.; WOODHEAD, R. J.; MATTHIESSEN, P. Polycyclic Aromatic Hydrocarbons (PAH) in seawater around England and Wales. Mar. Pollut. Bull., v. 34, n. 5, p. 306-322, 1997.

[26] LEE, R. F.; PAGE, D. S. Petroleum hydrocarbons and their effects in subtidal regions after major oil spills. Mar. Pollut. Bull., v. 34, n. 11, p. 928-940, 1997.

[27] LEE, R. F.; STEINERT, S. Use of the singles cell electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat. Res., v. 544, n. 1, p. 43-64, 2003.

[28] MALLAKIN, A.; DIXON, D. G.; GREENBERG, B. M. Pathway of anthracene modification under simulated solar radiation. Chemosphere, v. 40, n. 12, p. 1435-1441, 2000.

[29] MASKAOUI, K.; ZHOU, J. L.; HONG, H. S.; ZHANG, Z. L. Contamination by polycyclic aromatic hydrocarbons in the Jiulong River Estuary and Western Xiamen Sea, China. Environ. Pollut., v. 118, n.1, p. 109-122, 2002.

[30] MCELROY, A. E.; FARRINGTON, J. W.; TEAL, J. M. Bioavailability of polycyclic aromatic hydrocarbons in the aquatic environment. In: VARANASI, U. (Ed.) Metabolism of polycyclic aromatic hydrocarbons in the aquatic environment Boca Raton: CRC Press, 1989. p. 1-39.

[31] MEDEIROS, P. M.; BÍCEGO, M. C. Investigation of natural and anthropogenic hydrocarbon inputs in sediment using geochemical markers. II. São Sebastião, SP-Brazil. Mar. Pollut. Bull., v. 49, n. 11-12, p. 892-899, 2004.

[32] MEDEIROS, P. M.; BÍCEGO, M. C.; CASTELÃO, R. M.; DEL ROSSO, C.; FILMANN, G.; ZAMBONI, A. J. Natural and anthropogenic hydrocarbon inputs to sediments of Patos Lagoon Estuary, Brazil. Environ. Int., v. 31, n. 1, p. 77-87, 2005.

[33] MENEZES, N. A.; FIGUEIREDO, J. L. Manual de peixes marinhos do sudeste do Brasil. IV. Teleostei 3 São Paulo: Museu de Zoologia da Universidade de São Paulo, 1980. 96 p.

[34] MOHANTY, G.; MOHANTY, J.; NAYAK, A. K.; MOHANTY, S.; DUTTA, S. K. Application of comet assay in the study of DNA damage and recovery in rohu (Labeo rohita) fingerlings after an exposure to phorate, an organophosphate pesticide. Ecotoxicology, v. 20, n. 1, p. 283-292, 2011.

[35] NEFF, J. M. Polycyclic aromatic hydrocarbons in the aquatic environment: sources, fates and biological effects. London: Applied Science Publishers, 1979. 262 p.

[36] NIANG, T. M. S., PESSANHA, A. L. M.; ARAÚJO, F. G. Dieta de juvenis de Trachinotus carolinus (Actinopterygii, Carangidae) em praias arenosas na costa do Rio de Janeiro. Iheringia, Ser. Zool., v. 100, n. 1, p. 35-42, 2010.

[37] ORIS, J. T.; GIESY Jr., J. P. The photoenhanced toxicity of anthracene to juvenile sunfish (Lepomis spp.). Aquat. Toxicol., v. 6, n. 2, p. 133-146, 1985.

[38] ORIS, J. T.; GIESY Jr., J. P. The photo-induced toxicity of polycyclic aromatic hydrocarbons to larvae of the fathead minnow (Pimephales promelas). Chemosphere, v. 16, n. 7, p. 1395-1404, 1987.

[39] PACHECO, M.; SANTOS, M. A. Biotransformation, genotoxic, and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicol. Environ. Saf., v. 53, n. 3, p. 331-347, 2002.

[40] PELLETIER, E.; SARGIAN, P.; PAYET, J.; DEMERS, S. Ecotoxicological effects of combined UVB and organic contaminants in coastal waters: a review. Photochem. Photobiol., v. 82, n. 4, p. 981-993, 2006.

[41] RAND, G. M. Fish toxicity studies. In: DI GIULIO, R. T.; HINTON, D. E. (Eds.). The toxicology of fishes Boca Raton: CRC Press, 2008. p. 659-681.

[42] REN, H.; KAWAGOE, T.; JIA, H.; ENDO, H.; KITAZAWA, A.; GOTO, S.; HAYASHI, T. Continuous surface seawater surveillance on poly aromatic hydrocarbons (PAHs) and mutagenicity of East and South China Seas. Estuarine, Coastal Shelf Sci., v. 86, n. 3, p. 395-400, 2010.

[43] ROCHA, A. J. S.; SANTOS, T. C.; GOMES, V.; BÍCEGO, M. C.; BARBOSA, A. C. R. A.; PASSOS, M. J. A. C. R.; HASUE, F. M.; PHAN, V. N. Assessment of trophic transfer of benzo(a)pyrenegenotoxicity from the post-larval pink shrimp F. brasiliensis to juvenile Florida pompano T. carolinus Environ. Toxicol. Pharmacol., v. 34, n. 3, p. 969-976, 2012.

[44] SANTOS, T. C. A.; PHAN, V. N.; PASSOS, M. J. A. C. R.; GOMES, V. Effects of naphthalene on metabolic rate and ammonia excretion of juvenile Florida pompano, Trachinotus carolinus J. Exp. Mar. Biol. Ecol., v. 335, n. 1, p. 82-90, 2006.

[45] SCHIRMER, K.; CHAN, A. G. J.; GREENBERG, B. M.; DIXON, D. G.; BOLS, N. C. Ability of 16 priority PAHs to be photocytotoxic to a cell line from the rainbow trout Gill. Toxicology, v. 127, p. 143-155, 1998.

[46] SINGH, N. P.; MCCOY, M. T.; TICE, R. R.; SCHNEIDER; E. L.A simple technique for quantitation of low level of DNA damage in individual cells. Exp. Cell Res., v. 175, n. 1, p. 184-191, 1988.

[47] TICE, R. R.; AGURELL, E.; ANDERSON, D.; BURLINSON, B.; HARTMANN, A.; KOBAYASHI, H.; MIYAMAE, Y.; ROJAS, E.; RYU, J. C.; SASAKI, Y. F. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ. Mol. Mutagen., v. 35, n. 3, p. 206-221, 2000.

[48] TOSHIMA, K.; HASEGAWA, M.; SHIMIZU, J.; MATSUMURA, S. Molecular design, chemical synthesis and biological evaluation of anthracene-carbohydrate hybrids as novel DNA photocleaving and photoselective cytotoxic agents. ARKIVOC, v.2004, n.13, p. 28-35, 2004.

[49] TOYOOKA, T.; IBUKI, Y.DNA damage induced by coexposure to PAHs and light. Environ. Toxicol. Pharmacol., v. 23, n. 2, p. 256-263, 2007.

[50] ULUPINAR, M.; OKUMUS, I. Detection of mutagenic-carcinogenic pollutants in aquatic system using cytogenetic methods in fish. Turk. J. Zool., v. 26, p. 141-148, 2002.

[51] UNITED STATES. Department of Health and Human Services. Public Health Services. Agency for Toxic Substances and Disease Registry. Toxicological profile for polycyclic aromatic hydrocarbons Atlanta: Agency for Toxic Substances and Disease Registry, 1995. 30 p.

[52] VANZELLA, T. P.; MARTINEZ, C. B. R.; CÓLUS, I. M. S. Genotoxic and mutagenic effects of diesel oil water soluble fraction on a neotropical fish species. Mutat. Res., v. 631, n. 1, p. 36-43, 2007.

[53] VIEIRA, L. R.; SOUSA, A.; FRASCO, M. F.; LIMA, I.; MORGADO, F.; GUILHERMINO, L. Acute effects of Benzo[a]pyrene, anthracene and a fuel oil on biomarkers of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Sci. Total Environ., v. 395, n. 2/3, p. 87-100, 2008.

[54] VIGURI, J.; VERDE, J.; IRABIEN, A. Environmental assessment of polycyclic aromatic hydrocarbons (PAHs) in surface sediments of the Santander Bay, Northern Spain. Chemosphere, v. 48, n. 2, p. 157-165, 2002.

[55] ZAR, J. H. Biostatistical analysis 3.ed. Upper Saddle River: Prentice-Hall, 1996. 918 p.