Advertisement

Occurrence, sources and effects of polycyclic aromatic hydrocarbons in the Tunis lagoon, Tunisia: an integrated approach using multi-level biological responses in Ruditapes decussatus

  • Houssem ChalghmiEmail author
  • Jean-Paul Bourdineaud
  • Ikram Chbani
  • Zohra Haouas
  • Saida Bouzid
  • Hassan Er-Raioui
  • Dalila Saidane-Mosbahi
Multi-Stressors in Freshwater and Transitional Environments: from Legacy Pollutants to Emerging Ones
  • 52 Downloads

Abstract

Coastal lagoons are critical ecosystems presenting a strategic economic importance, but they are subjected to potential anthropogenic impact. As part of the Tunis lagoon (Tunisia) biomonitoring study, levels, composition pattern and sources of polycyclic aromatic hydrocarbons (PAHs) in surface sediments along with their bioavailability in clam Ruditapes decussatus were investigated in polluted (S2–S4) and reference (S1) sites. In order to investigate the contamination effects at different biological levels in clams, a wide set of biomarkers, including gene expression changes, enzymatic activities disruption and histopathological alterations, was analysed. Biomarkers were integrated in a biomarker index (IBR index) to allow a global assessment of the biological response. Principal component analysis (PCA) was used for chemical and biological data integration to rank the sampling sites according to their global environmental quality. Sediment PAHs levels ranged between 144.5 and 3887.0 ng g−1 dw in the Tunis lagoon sites versus 92.6 ng g−1 dw in the reference site. The high PAH concentrations are due to anthropogenic activities around the lagoon. PAH composition profiles and diagnostic isomer ratios analysis indicated that PAHs were of both pyrolitic and petrogenic origins. Clams sampled from S2 and S3 exhibited the highest PAH contents with 2192.6 ng g−1 dw and 2371.4 ng g−1 dw, respectively. Elevated levels of tissue PAHs were associated to an increase in biotransformation and antioxidant activities, and lipid peroxidation levels along with an overexpression of different genes encoding for general stress response, mitochondrial metabolism and antioxidant defence, in addition to the emergence of severe and diverse histopathological alterations in the clams’ digestive glands. IBR index was suitable for sampling sites ranking (S1 = 0 < S4 = 0.4 < S3 = 1.15 < S2 = 1.27) based on the level of PAH-induced stress in clams. PCA approach produced two components (PC1, 83.8% and PC2, 12.2%) that describe 96% of the variance in the data and thus highlighted the importance of integrating contaminants in sediments, their bioaccumulation and a battery of biomarkers of different dimensions for the assessment of global health status of coastal and lagoon areas.

Keywords

Tunis lagoon Biomonitoring Ruditapes decussatus Polycyclic aromatic hydrocarbons Multivariate analysis Multi-level approach Integrated biomarker response 

Notes

Acknowledgements

This study was supported by the University of Bordeaux, France, the Ministry of Scientific Research and Technology, the University of Monastir, Tunisia, and the French Institute of Tunisia.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11356_2019_4220_MOESM1_ESM.docx (4.6 mb)
ESM 1 (DOCX 4677 kb)

References

  1. Al Kaddissi S, Legeay A, Elia AC et al (2014) Mitochondrial gene expression, antioxidant responses, and histopathology after cadmium exposure. Environ Toxicol 29:893–907.  https://doi.org/10.1002/tox.21817 CrossRefGoogle Scholar
  2. Amiard J-C, Amiard-Triquet C, Barka S et al (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202.  https://doi.org/10.1016/j.aquatox.2005.08.015 CrossRefGoogle Scholar
  3. Au DWT (2004) The application of histo-cytopathological biomarkers in marine pollution monitoring: a review. Mar Pollut Bull 48:817–834.  https://doi.org/10.1016/j.marpolbul.2004.02.032 CrossRefGoogle Scholar
  4. Banni M, Bouraoui Z, Ghedira J, Clearandeau C, Jebali J, Boussetta H (2009) Seasonal variation of oxidative stress biomarkers in clams Ruditapes decussatus sampled from Tunisian coastal areas. Environ Monit Assess 155:119–128.  https://doi.org/10.1007/s10661-008-0422-3 CrossRefGoogle Scholar
  5. Banni M, Negri A, Dagnino A, Jebali J, Ameur S, Boussetta H (2010) Acute effects of benzo[a]pyrene on digestive gland enzymatic biomarkers and DNA damage on mussel Mytilus galloprovincialis. Ecotoxicol Environ Saf 73:842–848.  https://doi.org/10.1016/j.ecoenv.2009.12.032 CrossRefGoogle Scholar
  6. Baumard P, Budzinski H, Garrigues P, Sorbe JC, Burgeot T, Bellocq J (1998a) Concentrations of PAHs (polycyclic aromatic hydrocarbons) in various marine organisms in relation to those in sediments and to trophic level. Mar Pollut Bull 36:951–960.  https://doi.org/10.1016/S0025-326X(98)00088-5 CrossRefGoogle Scholar
  7. Baumard P, Budzinski H, Garrigues P (1998b) Polycyclic aromatic hydrocarbons in sediments and mussels of the western Mediterranean sea. Environ Toxicol Chem 17:765–776.  https://doi.org/10.1002/etc.5620170501 CrossRefGoogle Scholar
  8. Bebianno MJ, Barreira LA (2009) Polycyclic aromatic hydrocarbons concentrations and biomarker responses in the clam Ruditapes decussatus transplanted in the Ria Formosa lagoon. Ecotoxicol Environ Saf 72:1849–1860.  https://doi.org/10.1016/j.ecoenv.2009.03.016 CrossRefGoogle Scholar
  9. Bebianno MJ, Company R, Serafim A et al (2005) Antioxidant systems and lipid peroxidation in Bathymodiolus azoricus from Mid-Atlantic Ridge hydrothermal vent fields. Aquat Toxicol 75:354–373.  https://doi.org/10.1016/j.aquatox.2005.08.013 CrossRefGoogle Scholar
  10. Bebianno MJ, Pereira CG, Rey F, Cravo A, Duarte D, D'Errico G, Regoli F (2015) Integrated approach to assess ecosystem health in harbor areas. Sci Total Environ 514:92–107.  https://doi.org/10.1016/j.scitotenv.2015.01.050 CrossRefGoogle Scholar
  11. Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322.  https://doi.org/10.1002/etc.5620210629 CrossRefGoogle Scholar
  12. Bemanikharanagh A, Bakhtiari AR, Mohammadi J, Taghizadeh-Mehrjardi R (2017) Characterization and ecological risk of polycyclic aromatic hydrocarbons (PAHs) and n-alkanes in sediments of Shadegan international wetland, the Persian Gulf. Mar Pollut Bull 124:155–170.  https://doi.org/10.1016/j.marpolbul.2017.07.015 CrossRefGoogle Scholar
  13. Bi C, Wang X, Jia J, Chen Z (2018) Spatial variation and sources of polycyclic aromatic hydrocarbons influenced by intensive land use in an urbanized river network of East China. Sci Total Environ 627:671–680.  https://doi.org/10.1016/j.scitotenv.2018.01.272 CrossRefGoogle Scholar
  14. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  15. Breitwieser M, Thomas-Guyon H, Huet V, Sagerup K, Geraudie P (2018) Spatial and temporal impacts of the Skjervøy harbour diesel spill on native population of blue mussels: a sub-Arctic case study. Ecotoxicol Environ Saf 153:168–174.  https://doi.org/10.1016/j.ecoenv.2018.01.033 CrossRefGoogle Scholar
  16. Broeg K, Lehtonen KK (2006) Indices for the assessment of environmental pollution of the Baltic Sea coasts: integrated assessment of a multi-biomarker approach. Mar Pollut Bull 53:508–522.  https://doi.org/10.1016/j.marpolbul.2006.02.004 CrossRefGoogle Scholar
  17. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310CrossRefGoogle Scholar
  18. Cacciatore F, Bernarello V, Boscolo Brusà R, Sesta G, Franceschini G, Maggi C, Gabellini M, Lamberti CV (2018) PAH (polycyclic aromatic hydrocarbon) bioaccumulation and PAHs/shell weight index in Ruditapes philippinarum (Adams & Reeve, 1850) from the Vallona lagoon (northern Adriatic Sea, NE Italy). Ecotoxicol Environ Saf 148:787–798.  https://doi.org/10.1016/j.ecoenv.2017.11.050 CrossRefGoogle Scholar
  19. Cambier S, Bénard G, Mesmer-Dudons N, Gonzalez P, Rossignol R, Brèthes D, Bourdineaud JP (2009) At environmental doses, dietary methylmercury inhibits mitochondrial energy metabolism in skeletal muscles of the zebra fish (Danio rerio). Int J Biochem Cell Biol 41:791–799.  https://doi.org/10.1016/j.biocel.2008.08.008 CrossRefGoogle Scholar
  20. Capó X, Tejada S, Box A, Deudero S, Sureda A (2015) Oxidative status assessment of the endemic bivalve Pinna nobilis affected by the oil spill from the sinking of the Don Pedro. Mar Environ Res 110:19–24.  https://doi.org/10.1016/j.marenvres.2015.07.013 CrossRefGoogle Scholar
  21. Capolupo M, Franzellitti S, Kiwan A, Valbonesi P, Dinelli E, Pignotti E, Birke M, Fabbri E (2017) A comprehensive evaluation of the environmental quality of a coastal lagoon (Ravenna, Italy): integrating chemical and physiological analyses in mussels as a biomonitoring strategy. Sci Total Environ 598:146–159.  https://doi.org/10.1016/j.scitotenv.2017.04.119 CrossRefGoogle Scholar
  22. Chalghmi H, Zrafi I, Saidane-Mosbahi D (2015) Metabolism and oxidative stress biomarkers in clam Ruditapes decussatus to assess pollution in industrial area of Mediterranean lagoon. Int J Res Chem Environ 5:42–49Google Scholar
  23. Chalghmi H, Bourdineaud J-P, Haouas Z, Gourves PY, Zrafi I, Saidane-Mosbahi D (2016a) Transcriptomic, biochemical, and histopathological responses of the clam Ruditapes decussatus from a metal-contaminated Tunis lagoon. Arch Environ Contam Toxicol 70:241–256.  https://doi.org/10.1007/s00244-015-0185-0 CrossRefGoogle Scholar
  24. Chalghmi H, Zrafi I, Gourves P-Y, Bourdineaud JP, Saidane-Mosbahi D (2016b) Combined effects of metal contamination and abiotic parameters on biomarker responses in clam Ruditapes decussatus gills: an integrated approach in biomonitoring of Tunis lagoon. Environ Sci Process Impacts 18:895–907.  https://doi.org/10.1039/c6em00139d CrossRefGoogle Scholar
  25. Chalghmi H, Zrafi I, Saidane-Mosbahi D (2016c) Chronic effects of petroleum hydrocarbons in Tunis-navigation channel on phase I and II biotransformation enzymes in bivalve species. Int J Res Chem Environ 6:28–33Google Scholar
  26. Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) CRC handbook of methods for oxygen radical research. CRC Press Inc., Boca Raton, pp 283–284Google Scholar
  27. Costa PM, Carreira S, Costa MH, Caeiro S (2013) Development of histopathological indices in a commercial marine bivalve (Ruditapes decussatus) to determine environmental quality. Aquat Toxicol 126:442–454.  https://doi.org/10.1016/j.aquatox.2012.08.013 CrossRefGoogle Scholar
  28. Cuevas N, Zorita I, Costa PM, Franco J, Larreta J (2015) Development of histopathological indices in the digestive gland and gonad of mussels: integration with contamination levels and effects of confounding factors. Aquat Toxicol 162:152–164.  https://doi.org/10.1016/j.aquatox.2015.03.011 CrossRefGoogle Scholar
  29. Culotta L, De Stefano C, Gianguzza A et al (2006) The PAH composition of surface sediments from Stagnone coastal lagoon, Marsala (Italy). Mar Chem 99:117–127.  https://doi.org/10.1016/j.marchem.2005.05.010 CrossRefGoogle Scholar
  30. De La Torre-Roche RJ, Lee W-Y, Campos-Díaz SI (2009) Soil-borne polycyclic aromatic hydrocarbons in El Paso, Texas: analysis of a potential problem in the United States/Mexico border region. J Hazard Mater 163:946–958.  https://doi.org/10.1016/j.jhazmat.2008.07.089 CrossRefGoogle Scholar
  31. Devin S, Buffet PE, Châtel A, Perrein-Ettajani H, Valsami-Jones E, Mouneyrac C (2017) The integrated biomarker response: a suitable tool to evaluate toxicity of metal-based nanoparticles. Nanotoxicology 11:1–6.  https://doi.org/10.1080/17435390.2016.1269374 CrossRefGoogle Scholar
  32. dos Reis IMM, Mattos JJ, Garcez RC, Zacchi FL, Miguelão T, Flores-Nunes F, Toledo-Silva G, Sasaki ST, Taniguchi S, Bícego MC, Cargnin-Ferreira E, Bainy ACD (2015) Histological responses and localization of the cytochrome P450 (CYP2AU1) in Crassostrea brasiliana exposed to phenanthrene. Aquat Toxicol 169:79–89.  https://doi.org/10.1016/j.aquatox.2015.10.011 CrossRefGoogle Scholar
  33. Er-Raioui H, Bouzid S, Marhraoui M, Saliot A (2009) Hydrocarbon pollution of the Mediterranean coastline of Morocco. Ocean Coast Manag 52:124–129.  https://doi.org/10.1016/j.ocecoaman.2008.10.006 CrossRefGoogle Scholar
  34. Giannapas M, Karnis L, Dailianis S (2012) Generation of free radicals in haemocytes of mussels after exposure to low molecular weight PAH components: immune activation, oxidative and genotoxic effects. Comp Biochem Physiol Toxicol Pharmacol CBP 155:182–189.  https://doi.org/10.1016/j.cbpc.2011.08.001 CrossRefGoogle Scholar
  35. Gupta SC, Sharma A, Mishra M, Mishra RK, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377–384.  https://doi.org/10.1016/j.lfs.2009.12.015 CrossRefGoogle Scholar
  36. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  37. Kamel N, Burgeot T, Banni M, Chalghaf M, Devin S, Minier C, Boussetta H (2014) Effects of increasing temperatures on biomarker responses and accumulation of hazardous substances in rope mussels (Mytilus galloprovincialis) from Bizerte lagoon. Environ Sci Pollut Res 21:6108–6123.  https://doi.org/10.1007/s11356-014-2540-5 CrossRefGoogle Scholar
  38. Kim K-H, Jahan SA, Kabir E, Brown RJC (2013) A review of airborne polycyclic aromatic hydrocarbons (PAHs) and their human health effects. Environ Int 60:71–80.  https://doi.org/10.1016/j.envint.2013.07.019 CrossRefGoogle Scholar
  39. Krishnakumar PK, Asokan PK, Pillai VK (1990) Physiological and cellular responses to copper and mercury in the green mussel Perna viridis (Linnaeus). Aquat Toxicol 18:163–173.  https://doi.org/10.1016/0166-445X(90)90024-J CrossRefGoogle Scholar
  40. Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666.  https://doi.org/10.1016/S0025-326X(01)00060-1 CrossRefGoogle Scholar
  41. Long ER, Macdonald DD, Smith SL, Calder FD (1995) Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Manag 19:81–97.  https://doi.org/10.1007/BF02472006 CrossRefGoogle Scholar
  42. Lowe DM, Fossato VU (2000) The influence of environmental contaminants on lysosomal activity in the digestive cells of mussels (Mytilus galloprovincialis) from the Venice Lagoon. Aquat Toxicol 48:75–85.  https://doi.org/10.1016/S0166-445X(99)00054-5 CrossRefGoogle Scholar
  43. Lu M, Zeng D-C, Liao Y, Tong B (2012) Distribution and characterization of organochlorine pesticides and polycyclic aromatic hydrocarbons in surface sediment from Poyang Lake, China. Sci Total Environ 433:491–497.  https://doi.org/10.1016/j.scitotenv.2012.06.108 CrossRefGoogle Scholar
  44. Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30.  https://doi.org/10.1016/j.aquatox.2010.10.006 CrossRefGoogle Scholar
  45. Michel XR, Suteau P, Robertson LW, Narbonne J-F (1993) Effects of benzo(a)pyrene, 3,3′,4,4′-tetrachlorobiphenyl and 2,2′,4,4′,5,5′-hexachlorobiphenyl on the xenobiotic-metabolizing enzymes in the mussel (Mytilus galloprovincialis). Aquat Toxicol 27:335–344.  https://doi.org/10.1016/0166-445X(93)90062-6 CrossRefGoogle Scholar
  46. Michel XR, Beasse C, Narbonne J-F (1995) In vivo metabolism of benzo(a)pyrene in the mussel Mytilus galloprovincialis. Arch Environ Contam Toxicol 28:215–222.  https://doi.org/10.1007/BF00217619 CrossRefGoogle Scholar
  47. Mirsadeghi SA, Zakaria MP, Yap CK, Gobas F (2013) Evaluation of the potential bioaccumulation ability of the blood cockle (Anadara granosa L.) for assessment of environmental matrices of mudflats. Sci Total Environ 454–455:584–597.  https://doi.org/10.1016/j.scitotenv.2013.03.001 CrossRefGoogle Scholar
  48. Moore MN (1988) Cytochemical responses of the lysosomal system and NADPH-ferrihemoprotein reductase in molluscan digestive cells to environmental and experimental exposure to xenobiotics. Mar Ecol Prog Ser 46:81–89CrossRefGoogle Scholar
  49. Mrdaković M, Ilijin L, Vlahović M, Matić D, Gavrilović A, Mrkonja A, Perić-Mataruga V (2016) Acetylcholinesterase (AChE) and heat shock proteins (Hsp70) of gypsy moth (Lymantria dispar L.) larvae in response to long-term fluoranthene exposure. Chemosphere 159:565–569.  https://doi.org/10.1016/j.chemosphere.2016.06.059 CrossRefGoogle Scholar
  50. Mzoughi N, Chouba L (2011) Distribution and partitioning of aliphatic hydrocarbons and polycyclic aromatic hydrocarbons between water, suspended particulate matter, and sediment in harbours of the west coastal of the Gulf of Tunis (Tunisia). J Environ Monit 13:689–698.  https://doi.org/10.1039/C0EM00616E CrossRefGoogle Scholar
  51. Nicholson S, Lam PKS (2005) Pollution monitoring in Southeast Asia using biomarkers in the mytilid mussel Perna viridis (Mytilidae: Bivalvia). Environ Int 31:121–132.  https://doi.org/10.1016/j.envint.2004.05.007 CrossRefGoogle Scholar
  52. Orbea A, Ortiz-Zarragoitia M, Solé M, Porte C, Cajaraville MP (2002) Antioxidant enzymes and peroxisome proliferation in relation to contaminant body burdens of PAHs and PCBs in bivalve molluscs, crabs and fish from the Urdaibai and Plentzia estuaries (Bay of Biscay). Aquat Toxicol 58:75–98.  https://doi.org/10.1016/S0166-445X(01)00226-0 CrossRefGoogle Scholar
  53. OSPAR (2009) Background Document on CEMP Assessment Criteria for QSR 2010. OSPAR Commission 2009. Monitoring and Assessment Series, ISBN 978-1-907390-08-1, 25.Google Scholar
  54. Pérez-Ruzafa A, Marcos C, Pérez-Ruzafa IM (2011) Mediterranean coastal lagoons in an ecosystem and aquatic resources management context. Phys Chem Earth Parts ABC 36:160–166.  https://doi.org/10.1016/j.pce.2010.04.013 CrossRefGoogle Scholar
  55. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45–e445Google Scholar
  56. Powell RD, Goodenow DA, Mixer HV, Mckillop IH, Evans SL (2017) Cytochrome c limits oxidative stress and decreases acidosis in a rat model of hemorrhagic shock and reperfusion injury. J Trauma Acute Care Surg 82:35–41.  https://doi.org/10.1097/TA.0000000000001257 CrossRefGoogle Scholar
  57. Rajpara RK, Dudhagara DR, Bhatt JK, Gosai HB, Dave BP (2017) Polycyclic aromatic hydrocarbons (PAHs) at the Gulf of Kutch, Gujarat, India: occurrence, source apportionment, and toxicity of PAHs as an emerging issue. Mar Pollut Bull 119:231–238.  https://doi.org/10.1016/j.marpolbul.2017.04.039 CrossRefGoogle Scholar
  58. Riba I, González de Canales M, Forja JM, DelValls TA (2004) Sediment quality in the Guadalquivir estuary: sublethal effects associated with the Aznalcóllar mining spill. Mar Pollut Bull 48:153–163.  https://doi.org/10.1016/S0025-326X(03)00392-8 CrossRefGoogle Scholar
  59. Roesijadi G, Bogumil R, Vasák M, Kägi JHR (1998) Modulation of DNA binding of a tramtrack zinc finger peptide by the metallothionein-thionein conjugate pair. J Biol Chem 273:17425–17432.  https://doi.org/10.1074/jbc.273.28.17425 CrossRefGoogle Scholar
  60. Serafim A, Company R, Lopes B, Fonseca VF, França S, Vasconcelos RP, Bebianno MJ, Cabral HN (2012) Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems. Ecol Indic 19:215–225.  https://doi.org/10.1016/j.ecolind.2011.08.009 CrossRefGoogle Scholar
  61. Shaw GR, Connell DW (1994) Prediction and monitoring of the carcinogenicity of polycyclic aromatic compounds (PACs). In: Ware G.W. (eds), Reviews of environmental contamination and toxicology, vol 135. Springer, New York, NY, pp 1–62.  https://doi.org/10.1007/978-1-4612-2634-5_1
  62. Sheir SK, Handy RD (2010) Tissue injury and cellular immune responses to cadmium chloride exposure in the common mussel Mytilus edulis: modulation by lipopolysaccharide. Arch Environ Contam Toxicol 59:602–613.  https://doi.org/10.1007/s00244-010-9502-9 CrossRefGoogle Scholar
  63. Tuncel SG, Topal T (2015) Polycyclic aromatic hydrocarbons (PAHs) in sea sediments of the Turkish Mediterranean coast, composition and sources. Environ Sci Pollut Res 22:4213–4221.  https://doi.org/10.1007/s11356-014-3621-1 CrossRefGoogle Scholar
  64. Usheva LN, Vaschenko MA, Durkina VB (2006) Histopathology of the digestive gland of the bivalve mollusk Crenomytilus grayanus (Dunker, 1853) from southwestern Peter the Great Bay, Sea of Japan. Russ J Mar Biol 32:166–172.  https://doi.org/10.1134/S1063074006030047 CrossRefGoogle Scholar
  65. Wurl O, Obbard JP (2004) A review of pollutants in the sea-surface microlayer (SML): a unique habitat for marine organisms. Mar Pollut Bull 48:1016–1030.  https://doi.org/10.1016/j.marpolbul.2004.03.016 CrossRefGoogle Scholar
  66. Xie J, Zhao C, Han Q, Zhou H, Li Q, Diao X (2017) Effects of pyrene exposure on immune response and oxidative stress in the pearl oyster, Pinctada martensii. Fish Shellfish Immunol 63:237–244.  https://doi.org/10.1016/j.fsi.2017.02.032 CrossRefGoogle Scholar
  67. Xiu M, Pan L, Jin Q (2014) Bioaccumulation and oxidative damage in juvenile scallop Chlamys farreri exposed to benzo[a]pyrene, benzo[b]fluoranthene and chrysene. Ecotoxicol Environ Saf 107:103–110.  https://doi.org/10.1016/j.ecoenv.2014.05.016 CrossRefGoogle Scholar
  68. Zaghden H, Tedetti M, Sayadi S, Serbaji MM, Elleuch B, Saliot A (2017) Origin and distribution of hydrocarbons and organic matter in the surficial sediments of the Sfax-Kerkennah channel (Tunisia, southern Mediterranean Sea). Mar Pollut Bull 117:414–428.  https://doi.org/10.1016/j.marpolbul.2017.02.007 CrossRefGoogle Scholar
  69. Zrafi I, Hizem L, Chalghmi H, Ghrabi A, Rouabhia M, Saidane-Mosbahi D (2013) Aliphatic and aromatic biomarkers for petroleum hydrocarbon investigation in marine sediment. J Pet Sci Res 2:145–155.  https://doi.org/10.14355/jpsr.2013.0204.01 Google Scholar
  70. Zrafi-Nouira I, Khedir-Ghenim Z, Zrafi F, Bahri R, Cheraeif I, Rouabhia M, Saidane-Mosbahi D (2008) Hydrocarbon pollution in the sediment from the Jarzouna-Bizerte coastal area of Tunisia (Mediterranean Sea). Bull Environ Contam Toxicol 80:566–572.  https://doi.org/10.1007/s00128-008-9421-x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.UMR CNRS 5805 EPOCUniversity of BordeauxArcachonFrance
  2. 2.Laboratory of Analysis Treatment and Valorization of Environmental Pollutants and Products, Faculty of Pharmacy, University of MonastirMonastirTunisia
  3. 3.Laboratory of Environment, Oceanology and Natural Resources, Faculty of Sciences and TechnologyUniversity of Abdelmalek EssaâdiTangierMorocco
  4. 4.Laboratory of Histology Cytology and Genetics, Faculty of Medicine, University of MonastirMonastirTunisia

Personalised recommendations