Skip to main content
SpringerLink
Log in

Genotoxicity and histological alterations in grey mullet Mugil liza exposed to petroleum water-soluble fraction (PWSF)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Petroleum hydrocarbons are considered one of the main organic chemicals found in water bodies. In the present study, the median lethal concentration (LC50) was estimated for mullet Mugil liza after acute exposure to petroleum water-soluble fraction (PWSF). Furthermore, histopathological studies and micronuclei frequency were also performed in order to observe deleterious effects of medium-term exposition to PWSF. Mullets (25 ± 2.3 g) were exposed to chronic concentrations (1.7, 3.5 and 7 % of PWSF), plus the control group, for 14 and 7 days of clearance time. Throughout the experimental period (1, 4, 14 and 21 days), blood samples were collected for analysis of micronucleus (MN) and liver and gills for histopathological study. For these procedures, seven fish were sampled per concentration tested. The LC50-96 h was estimated at 37.5 % of the PWSF. The time required for MN induction was 96 h of exposure. The time of clearance was sufficient to achieve a MN frequency similar to that of the control group. Histopathological studies showed severe changes in the gill and liver tissues. The most relevant histopathology in the gills was telangiectasia. Hepatic histopathology such as cholestasis, dilated sinusoids and inflammatory infiltrates were commonly described. The MN test and histological study effectively detected damages caused by medium-term exposition to the PWSF, and despite the toxicity, a few days without exposure can minimize PWSF genotoxicity in juveniles of M. liza.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Al-Sabti K, Metcalfe CD (1995) Fish micronuclei for assessing genotoxicity in water. Mutat Res 343:121–135

    Article  CAS  Google Scholar 

  • Álvarez LS, Bellas J, Nieto O, Bayona JM, Albaigés J, Beiras R (2008) Toxicity and phototoxicity of water-accommodated fraction obtained from Prestige fuel oil and Marine fuel oil evaluated by marine bioassays. Sci Total Environ 394:275–282

    Article  Google Scholar 

  • Anderson JW, Neff JM, Cox BA, Tatem HE, Hightower GM (1974) Characteristics of dispersions and water-soluble extracts of crude and refined oils and their toxicity to estuarine crustaceans and fish. Mar Biol 27:75–88

    Article  CAS  Google Scholar 

  • Ayllon F, Garcia-Vazquez E (2002) 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 467:177–186

    Google Scholar 

  • Barra R, Popp P, Quiroz R, Treutler H, Araneda A, Bauer C, Urrutia R (2006) Polycyclic aromatic hydrocarbons fluxes during the past 50 years observed in dated sediment cores from Andean mountain lakes in central south Chile. Ecotoxicol Environ Saf 63:52–60

    Article  CAS  Google Scholar 

  • Baršiene J, Lazutka J, Šyvokiene J, Dedonyte V, Rybakovas A, Bjornstad A, Andersen OK (2004) Analysis of micronuclei in blue mussels and fish from the Baltic and the North Seas. Environ Toxicol 19:365–371

    Article  Google Scholar 

  • Brand DG, Fink R, Bengeyfield W, Birtwell IK, Mcallister CD (2001) Salt water-acclimated pink salmon fry (Oncorrhynchus gorbuscha) develop stress-related visceral lesions after 10-day exposure to sublethal concentrations of the water-soluble fraction of North Slope crude oil. Toxicol Pathol 29(5):574–584

    Article  CAS  Google Scholar 

  • Buhler DR, Williams DE (1988) The role of biotransformation in the toxicity of chemicals. Aquatic Toxicol 11:19–28

    Article  CAS  Google Scholar 

  • Budzinsky H, Mazéas O, Tronczynski J, Désaunay Y, Bocquené G, Claireaux G (2004) Link between exposure of fish (Solea solea) to PAHs and metabolites: Application to the “Erika” oil spill. Aquat Living Resour 17:329–334

    Google Scholar 

  • Cajaraville MP, Bebianno JM, Blasco J, Porte C, Sarasquete C, Viarengo A (2000) The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ 247:295–311

    Article  CAS  Google Scholar 

  • Cavas T, Garanko NN, Arkhipchuk VV (2005) Induction of micronuclei and binuclei in blood, gill and liver cells of fishes subchronically exposed to cadmium chloride and copper sulphate. Food Chem Toxicol 43:569–574

    Article  CAS  Google Scholar 

  • Cohen AM, Nugegoda D (2000) Toxicity of three oil spill remediation techniques to the Australian bass Macquaria novemaculeata. Ecotoxicol Environ Saf 47:178–185

    Article  CAS  Google Scholar 

  • Costa PM, Diniz MS, Caeiro S, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, Delvalls A, Costa MH (2009) Histological biomarkers in liver and gills of juvenile Solea senegalensis exposed to contaminated estuarine sediments: a weighted indices approach. Aquat Toxicol 92:202–212

    Article  CAS  Google Scholar 

  • Cristaldi M, Ieradi LA, Udroiu I, Zilli R (2004) Comparative evaluation of background micronucleus frequencies in domestic mammals. Mut Res 559:1–9

    Article  CAS  Google Scholar 

  • Dórea HS, Bispo JRL, Aragão KAS, Cunha BB, Navickiene S, Alves JPH, Romão L, Garcia C (2007) Analysis of BTEX, PAHs and metals in the oilfield produced water in the State of Sergipe, Brazil. J Microchem 85:234–238

    Article  Google Scholar 

  • Fanta E, Rios FS, Romão S, Vianna ACC, Freiberger S (2003) Histopathology of the fish Corydoras paleatus contaminated with sublethal levels of organophosphorus in water and food. Ecotoxicol Environ Saf 54:119–130

    Article  CAS  Google Scholar 

  • Ferraro MVM, Fenocchio AS, Mantovani MS, Oliveira RC, Cestari MM (2004) Mutagenic effects of tributyltin and inorganic lead (Pb II) on the fish H. malabaricus as evaluated using the comet assay and the piscine micronucleus and chromosome aberration tests. Genet Mol Biol 27(1):103–107

    Article  CAS  Google Scholar 

  • Goksoyr A, Förlin L (1992) The cytochrome P-450 system in fish, aquatic toxicology and environmental monitoring. Aquat Toxicol 22:287–312

    Article  Google Scholar 

  • Gusmão EP, Rodrigues RV, Moreira CB, Romano LA, Sampaio LA, Miranda-Filho KC (2012) Growth and histopathological effects of chronic exposition of marine pejerrey Odontesthes argentinensis larvae to petroleum water-soluble fraction (WSF). Ambio 41:456–466

    Article  Google Scholar 

  • Gustavino B, Scornajjenghi KA, Minissi S, Ciccotti E (2001) Micronuclei induced in erythrocytes of Cyprinus carpio (teleostei, pisces) by X-ray and colchicine. Mutat Res Genet Toxicol Environ Mutagen 494:151–159

    Article  CAS  Google Scholar 

  • Haensly WE, Neff JM, Sharp JR, Morris AC, Bedgood MF, Boem PD (1982) Histopathology of Pleuronectes platessa L. from Amber Wrach and Amber Benoit, Brittany, France: long-term effects of the Amoco Cadiz crude oil spill. J Fish Dis 5:365–391

    Article  Google Scholar 

  • Hamilton MA, Russo RC, Thurston RV (1977) Trimmed Spearman–Karber Method for estimating median lethal concentrations in toxicity bioassays. Environ Sci Technol 11:714–719

    Article  CAS  Google Scholar 

  • Heath AG (1995) Water Pollution and Fish Physiology, 2nd edn. Lewis Publishers, Boca Raton

    Google Scholar 

  • Hylland K (2006) Polycyclic aromatic hydrocarbon (PAH) ecotoxicology in marine ecosystems. J Toxicol Environ Health A 69:109–123

    Article  CAS  Google Scholar 

  • Khan RA (2003) Health of flatfish from localities in Placentia Bay, Newfoundland, Contaminated with petroleum and PCBs. Arch Environ Contam Toxicol 44:485–492

    Article  CAS  Google Scholar 

  • Klobucar GI, Pavlica M, Erben R, Papes D (2003) Application of the micronucleus and comet assays to mussel Dreissena polymorpha haemocytes for genotoxicity monitoring of freshwater environments. Aquat Toxicol 64:15–23

    Article  CAS  Google Scholar 

  • Kumar R, Nagpure NS, Kushwaha B, Srivastava SK, Lakra WS (2009) Investigation of the genotoxicity of malathion to freshwater teleost fish Channa punctatus (Bloch) using the micronucleus test and comet assay. Arch Environ Contam Toxicol 58(1):123–130

    Article  Google Scholar 

  • Mazon AF, Cerqueira CCC, Fernandes MN (2002) Gill cellular changes induced by copper exposure in the South American tropical freshwater fish Prochilodus scrofa. Environ Res 88:52–63

    Article  CAS  Google Scholar 

  • Meier JR, Vernsing P, Torsella J (1999) Feasibility of micronucleus methods for monitoring genetic damage in two feral species of small mammals. Environ Mol Mutagen 33:219–225

    Article  CAS  Google Scholar 

  • Menezes NA, Figueiredo JL (1985) Manual de peixes marinhos do sudeste do Brasil, vol V, Teleostei (4). Museu de Zoologia da Universidade de São Paulo, São Paulo

    Google Scholar 

  • Menezes NA, Oliveira C, Nirchio M (2010) An old taxonomic dilemma: the identity of the western south Atlantic lebranche mullet (Teleostei: Perciformes: Mugilidae). Zootaxa 2519:59–68

    Google Scholar 

  • Myers MS, Johnson LL, Olson OP, Stehr CM, Horness BH, Collier TK, McCain BB (1998) Toxicopathic hepatic lesions as biomarkers of chemical contaminant exposure and effects in marine bottom fish species from the northeast and Pacific Coast, USA. Mar Pollut Bull 37:92–113

    Article  CAS  Google Scholar 

  • Nebert DW, Gonzalez FJ (1987) P450 genes: structure, evolution, and regulation. Annu Rev Biochem 6:945–993

    Article  Google Scholar 

  • Neff JM, Ostazeski S, Gardiner W, Stejskal I (2000) Effects of weathering on the toxicity of three offshore Australian crude oils and diesel fuel to marine animals. Environ Toxicol Chem 19(7):1809–1821

    Article  CAS  Google Scholar 

  • Nero V, Farwell A, Lister A, Van Der Kraak G, Lee LEJ, Van Meer T, MacKinnon MD, Dixon DG (2006) Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sand process-affected water. Ecotoxicol Environ Saf 63:365–377

    Article  CAS  Google Scholar 

  • Newman MC (2009) Fundamentals of Ecotoxicology. CRC Press, Virginia

    Google Scholar 

  • Nikinma M, Oikari A (1982) Physiological changes in trout (Salmo gairdneri) during a short-term exposure to resin acids and during recovery. Toxicol Lett 14:103–110

    Article  Google Scholar 

  • Pacheco M, Santos MA (2002) Naphthalene and ß-Naphthoflavone effects on Anguilla anguilla L. hepatic metabolism and erythrocytic nuclear abnormalities. Environ Int 28:285–293

    Article  CAS  Google Scholar 

  • Rand GM, Petrocelli SR (1985) Fundamentals of Aquatic Toxicology: Methods and Applications. Hemisphere Publishing Corporation, New York

    Google Scholar 

  • Ribeiro LR, Salvadori DMF, Marques EK (2003) Mutagênese Ambiental. Editora ULBRA, Canoas

    Google Scholar 

  • Rice SD (1985) Effects of oil on fish. In: Engelhardt FR (ed) Petroleum Effects in the Arctic Environment. Applied Science Publishers Ltd., London, pp 157–182

    Google Scholar 

  • Rodrigues RV, Miranda-Filho KC, Gusmão EP, Moreira CB, Romano LA, Sampaio LA (2010) Deleterious effects of water-soluble fraction of petroleum, diesel and gasoline on marine pejerrey Odontesthes argentinensis larvae. Sci Total Environ 408:2054–2059

    Article  CAS  Google Scholar 

  • Romano LA, Cueva FC (1988) Lesiones histologicas branquiales atribuibles a tóxicos en Odonthestes bonariensis (Pisces, Atherinidae). Rev Assoc Sci Nat Litor St Tome 19:135–142

    Google Scholar 

  • Romano LA, Lucchini L, Alvarez M, Wicky G, Huidobro SP, Marozzi A (2006) Distribuición de células granulares eosinófilas en Prochilodus platensis y sus características tintoriales. CIVA 24–31

  • Saeed T, Mutairi MA (1999) Chemical composition of the water soluble fraction of leaded gasolines in sea water. Environ Int 25:117–129

    Article  CAS  Google Scholar 

  • Schwaige J, Wanke R, Adam S, Pawert M, Honnen W, Triebskorn R (1997) The use of histopathological indicators to evaluate contaminant-related stress in fish. J Aquat Ecosyst Stress Recover 6:75–86

    Article  Google Scholar 

  • Silva CA, Oliveira Ribeiro CA, Katsumiti A, Araújo MLP, Zandoná EM, Costa Silva GP, Maschio J, Roche H, Silva de Assis HC (2009) Evaluation of waterborne exposure to oil spill 5 years after an accident in Southern Brazil. Ecotoxicol Environ Saf 72:400–409

    Article  CAS  Google Scholar 

  • Simonato JD, Guedes CLB, Martinez CBR (2008) Biochemical, physiological, and histological changes in the neotropical fish Prochilodus lineatus exposed to diesel oil. Ecotoxicol Environ Saf 69(1):112–120

    Article  CAS  Google Scholar 

  • Sindermann CJ (1979) Pollution-associated diseases and abnormalities of fish and shellfish: a review. Fish Bull 76:717–749

    Google Scholar 

  • Singer MM, Aurand D, Bragin GE, Clark JR, Coelho GM, Sowby ML, Tjeerdema RS (2000) Standardization of the preparation and quantification of water-accommodated fractions of petroleum for toxicity testing. Mar Pollut Bull 40:1007–1016

    Article  CAS  Google Scholar 

  • Solangi MA, Overstreet RM (2006) Histopathological changes in two estuarine fishes, Menidia beryllina (Cope) and Trinectes maculatus (Bloch and Schneider), exposed to crude oil and its water-soluble fractions. J Fish Dis 5:13–35

    Article  Google Scholar 

  • Sprague JB (1971) Measurement of pollutant toxicity to fish—III sublethal effects and safe concentrations. Water Res 5:245–266

    Article  CAS  Google Scholar 

  • Stephens SM, Alkindi AYA, Waring CP, Brown JA (1997) Corticosteroid and thyroid responses of larval and juvenile turbot exposed to the water-soluble fraction of crude oil. J Fish Biol 50:953–964

    Article  CAS  Google Scholar 

  • Tuvikene A, Huuskonen S, Koponen K, Ritola O, Mauer U, Lindströn-Seppa P (1999) Oil shale processing as a source of aquatic pollution: monitoring of the biologic effects in caged and feral freshwater fish. Environ Health Perspect 107:745–752

    Article  CAS  Google Scholar 

  • Vanzella TP, Martinez CBR, Cólus IMS (2007) Genotoxic and mutagenic effects of diesel oil water-soluble fraction on a tropical fish species. Mutat Res 631:36–43

    Article  CAS  Google Scholar 

  • Varanasi U (1989) Metabolism of polycyclic aromatic hydrocarbons in aquatic environment. CRC Press, Boca Raton, Florida, p 341

  • Yadav KK, Trivedi SP (2009) Sublethal exposure of heavy metals induces micronuclei in fish, Channa punctata. Chemosphere 77:1495–1500

    Article  CAS  Google Scholar 

  • Ziolli RL, Jardim WF (2002) Operational problems related to the preparation of the seawater soluble fraction of crude oil. J Environ Monit 4:138–141

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to gratefully acknowledge the Brazilian National Agency of Petroleum (ANP) for supporting the student C.B. Moreira. R.V. Rodrigues is supported by Brazilian CNPq. L.A. Sampaio is a research fellow of Brazilian CNPq (308013/2009-3). K.C. Miranda-Filho thanks CNPq (481613/2007-2) and CAPES for their support.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Aquicultura, Laboratório de Piscicultura Estuarina e Marinha, Universidade Federal do Rio Grande, CEP 96201-900, Rio Grande, RS, Brazil

    Cauê Bonucci Moreira, Ricardo Vieira Rodrigues & Emeline Pereira Gusmão

  2. Laboratório de Piscicultura Estuarina e Marinha, Instituto de Oceanografia, Universidade Federal do Rio Grande, CEP 96201-900, Rio Grande, RS, Brazil

    Luis Alberto Romano & Luís André Sampaio

  3. Laboratório de Ecotoxicologia e Microcontaminantes Orgânicos, Instituto de Oceanografia, Universidade Federal do Rio Grande, CEP 96201-900, Rio Grande, RS, Brazil

    Bianca Hartwig Seyffert

  4. Laboratório de Aquacultura, Departamento de Zootecnia, Escola de Veterinária, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, CEP 31270-901, Belo Horizonte, MG, Brazil

    Kleber Campos Miranda-Filho

Authors
  1. Cauê Bonucci Moreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ricardo Vieira Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Luis Alberto Romano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emeline Pereira Gusmão
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bianca Hartwig Seyffert
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luís André Sampaio
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kleber Campos Miranda-Filho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kleber Campos Miranda-Filho.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table 1

Mean values (±standard error) of water quality parameters during the evaluation of acute toxicity with PWSF for grey mullet Mugil liza juveniles. (DOCX 15 kb)

Table 2

Mean values (±standard error) of the water quality parameters during the evaluation of the chronic toxicity of petroleum WSF for juvenile grey mullet Mugil liza. (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Moreira, C.B., Rodrigues, R.V., Romano, L.A. et al. Genotoxicity and histological alterations in grey mullet Mugil liza exposed to petroleum water-soluble fraction (PWSF). Environ Sci Pollut Res 21, 5565–5574 (2014). https://doi.org/10.1007/s11356-013-2440-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-2440-0

Keywords

Search

Navigation