Abstract
Toxicity caused by exposure to pollutants from marine sediments is a consequence of the interaction between biota and xenobiotics most frequently released by anthropogenic activities. The present work intended to characterize the toxicity of natural sediments putatively impacted by distinct human activities, collected at several sites located in the south of the Gulf of Gabes, Zarzis area, Tunisia. The selected toxicity criteria were analysed following ecologically relevant test conditions. Organisms of the polychaete species Hediste diversicolor were chronically exposed (28 days) to the mentioned sediments. Toxicity endpoints were biomarkers involved in the toxic response to common anthropogenic chemicals, namely neurotoxic (acetylcholinesterase), anti-oxidant (catalase, glutathione peroxidase), metabolic (glutathione S-transferases) enzymatic activities, and oxidative damage (lipid peroxidation, TBARS assay). The chemical characterization of sediments showed that the samples collected from the site near an aquaculture facility were highly contaminated by heavy metals (Cd, Cu, Cr, Hg, Pb, and Zn) and polycyclic aromatic hydrocarbons (fluorene, phenanthrene, anthracene, fluoranthene and pyrene). H. diversicolor individuals exposed to the sediments from this specific site showed the highest values among all tested biomarkers, suggesting that these organisms were possibly under a pro-oxidative stress condition potentially promoted by anthropogenic pollution. Moreover, it was possible to conclude that individuals of the polychaete species H. diversicolor responded to the chronic exposure to potentially contaminated sediments from the southeast coast of Tunisia, eliciting adaptive responses of significant biological meaning.
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References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3
Ait Alla A, Mouneyrac C, Durou C, Moukrim A, Pellerin J (2006) Tolerance and biomarkers as useful tools for assessing environmental quality in the Oued Souss estuary (Bay of Agadir, Morocco). Comp Biochem Physiol Part C: Toxicol Pharmacol 143(1):23–29. https://doi.org/10.1016/j.cbpc.2005.11.015
Akcil A, Erust C, Ozdemiroglu S, Fonti V, Beolchini F (2015) A review of approaches and techniques used in aquatic contaminated sediments: metal removal and stabilization by chemical and biotechnological processes. J Clean Prod 86:24–36. https://doi.org/10.1016/j.jclepro.2014.08.009
Al-Gubory KH, Garrel C, Faure P, Sugino N (2012) Roles of antioxidant enzymes in corpus luteum rescue from reactive oxygen species-induced oxidative stress. Reprod Biomed Online 25(6):551–560. https://doi.org/10.1016/j.rbmo.2012.08.004
Almroth BC, Sturve J, Berglund Å, Förlin L (2005) Oxidative damage in eelpout (Zoarces viviparus), measured as protein carbonyls and TBARS, as biomarkers. Aquat Toxicol 73(2):171–180. https://doi.org/10.1016/j.aquatox.2005.03.007
Amado LL, Da Rosa CE, Leite AM, Moraes L, Vaz W, Lea GL, Martinez C, Geracitano LA (2006) 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 52(2):199–206. https://doi.org/10.1016/j.marpolbul.2005.11.006
Banni M, Bouraoui Z, Ghedira J, Clerandeau C, Guerbej H, Narbonne JF, Boussetta H (2009a) Acute effects of benzo[a]pyrene on liver phase I and II enzymes, and DNA damage on sea bream Sparus aurata. Fish Physiol Biochem 35(2):293–299. https://doi.org/10.1007/s10695-008-9210-9
Banni M, Bouraoui Z, Clerandeau C, Narbonne JF, Boussetta H (2009b) Mixture toxicity assessment of cadmium and benzo [a] pyrene in the sea worm Hediste diversicolor. Chemosphere 77(7):902–906. https://doi.org/10.1016/j.chemosphere.2009.08.041
Banni M, Chouchene L, Said K, Kerkeni A, Messaoudi I (2011) Mechanisms underlying the protective effect of zinc and selenium against cadmium-induced oxidative stress in zebrafish Danio rerio. Biometals 24(6):981–992. https://doi.org/10.1007/s10534-011-9456-z
Barhoumi B, Clérandeau C, Gourves PY, Le Menach K, Megdiche Y, Peluhet L, Budzinski H, Baudrimont M, Driss MR, Cachot J (2014) Pollution biomonitoring in the Bizerte lagoon (Tunisia), using combined chemical and biomarker analyses in grass goby, Zosterisessor ophiocephalus (Teleostei, Gobiidae). Mar Environ Res 101(1):184–195. https://doi.org/10.1016/j.marenvres.2014.07.002
Bergayou H, Mouneyrac C, Pellerin J, Moukrim A (2009) Oxidative stress responses in bivalves (Scrobicularia plana, Cerastoderma edule) from the Oued Souss estuary (Morocco). Ecotoxicol Environ Saf 72(3):765–769. https://doi.org/10.1016/j.ecoenv.2008.09.012
Beyer J, Sandvik M, Hylland K, Fjeld E, Egaas E, Aas E, Skåre JU, Goksøyr A (1996) Contaminant accumulation and biomarker responses in flounder (Platichthys flesus L.) and Atlantic cod (Gadus morhua L.) exposed by caging to polluted sediments in Sørfjorden, Norway. Aquat Toxicol 36(1–2):75–98. https://doi.org/10.1016/S0166-445X(96)00798-9
Bouraoui Z, Banni M, Ghedira J, Clerandeau C, Narbonne JF, Boussetta H (2009) Evaluation of enzymatic biomarkers and lipoperoxidation level in Hediste diversicolor exposed to copper and benzo[a]pyrene. Ecotoxicol Environ Saf 72(7):1893–1898. https://doi.org/10.1016/j.ecoenv.2009.05.011
Bouraoui Z, Banni M, Chouba L, Ghedira J, Clerandeau C, Jebali J, Narbonne JF, Boussetta H (2010) Monitoring pollution in Tunisian coasts using a scale of classification based on biochemical markers in worms Nereis (Hediste) diversicolor. Environ Monit Assess 164(1–4):691–700. https://doi.org/10.1007/s10661-009-0921-x
Bouraoui Z, Ghedira J, Boussetta H (2015) Biomarkers responses in different body regions of the polychaeta Hediste diversicolor (Nereidae, Polychaete) exposed to copper. Rev Gestão Costeira Integr J Integr Coast Zone Manage 15(3). https://doi.org/10.5894/rgci594
Bouraoui Z, Ghedira J, Banni M, Boussetta H (2016) Acute effects of cadmium and copper on cytochemical responses in the polychaete Hediste diversicolor. Int J Environ Res 10(1):131–138. https://doi.org/10.22059/IJER.2016.56895
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310. https://doi.org/10.1016/S0076-6879(78)52032-6
Buffet PE, Poirier L, Zalouk-Vergnoux A, Lopes C, Amiard JC, Gaudin P, de Faverneye CR, Guibbolini M, Gilliland D, Ettajani HP, Valsami-Jones E (2014) Biochemical and behavioural responses of the marine polychaete Hediste diversicolor to cadmium sulfide quantum dots (CdS QDs): waterborne and dietary exposure. Chemosphere 100:63–70. https://doi.org/10.1016/j.chemosphere.2013.12.069
Catalano B, Moltedo G, Martuccio G, Gastaldi L, Virno-Lamberti C, Lauria A, Ausili A (2012) Can Hediste diversicolor (Nereidae, Polychaete) be considered a good candidate in evaluating PAH contamination? A multimarker approach. Chemosphere 86(9):875–882. https://doi.org/10.1016/j.chemosphere.2011.10.040
CTA, Centre Technique d’Aquaculture (2017) Guide des fermes aquacoles en Tunisie, Tunisie, 50
Chassé C, Glémarec M (1976) Principes généraux de la classification des fonds pour la cartographie biosédimentaire. J Rech Océanogr 1(3):1–18
Cherif N, Attia El Hili H, Mzoughi N, Chouba L, El Bourl M, El-Amri D, Hamza A, Maatoug K, Zaafrane S, Hammami S (2011) Tunisian aquaculture: present situation and potentialities. Fish Farms Manage Dis Control Environ 1(4):1–19
Choi J, Oris JT (2000) Evidence of oxidative stress in bluegill sunfish (Lepomis macrochirus) liver microsomes simultaneously exposed to solar ultraviolet radiation and anthracene. Environ Toxicol Chem 19(7):1795–1799. https://doi.org/10.1002/etc.5620190713
Cognetti G, Maltagliati F (2000) Biodiversity and adaptive mechanisms in brackish water fauna. Mar Pollut Bull 40(1):7–14. https://doi.org/10.1016/S0025-326X(99)00173-3
Coll M, Piroddi C, Steenbeek J, Kaschner K, Lasram FBR, Aguzzi J, Ballesteros E, Bianchi CN, Corbera J, Dailianis T, Danovaro R, Estrada M, Froglia C, Galil BS, Gasol JM, Gertwagen R, Gil J, Guilhaumon F, Kesner-Reyes k, Kitsos MS, Koukouras A, Lampadariou N, Laxamana E, López-Fé de la Cuadra CF, Lotze hk, Martin D, Mouillot D, Oro D, Raicevich S, Rius-Barile J, Saiz-Salinas JI, San Vicente C, Somot, S, Templado J, Turon X, Vafidis D, Villanueva R, Voultsiadou E (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5(8). https://doi.org/10.1371/journal.pone.0011842
de Lima D, Roque GM, de Almeida EA (2013) In vitro and in vivo inhibition of acetylcholinesterase and carboxylesterase by metals in zebrafish (Danio rerio). Mar Environ Res 91:45–51. https://doi.org/10.1016/j.marenvres.2012.11.005
Deponte M (2013) Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta (BBA)-Gen Subj 1830(5):3217–3266. https://doi.org/10.1016/j.bbagen.2012.09.018
Drira Z, Elloumi J, Guermazi W, Hassen MB, Hamza A, Ayadi H (2014) Seasonal changes on planktonic diatom communities along an inshore-offshore gradient in the Gulf of Gabes (Tunisia). Acta Ecol Sin 34(1):34–43. https://doi.org/10.1016/j.chnaes.2013.11.005
Drira Z, Kmiha-Megdiche S, Sahnoun H, Hammami A, Allouche N, Tedetti M, Ayadi H (2016) Assessment of anthropogenic inputs in the surface waters of the southern coastal area of Sfax during spring (Tunisia, Southern Mediterranean Sea). Mar Pollut Bull 104(1–2):355–363. https://doi.org/10.1016/j.marpolbul.2016.01.035
Durou C, Mouneyrac C, Amiard-Triquet C (2005) Tolerance to metals and assessment of energy reserves in the polychaete Nereis diversicolor in clean and contaminated estuaries. Environ Toxicol 20(1):23–31. https://doi.org/10.1002/tox.20074
Durou C, Poirier L, Amiard J-C, Budzinski H, Gnassia-Barelli M, Lemenach K, Peluhet L, Mouneyrac C, Roméo M, Amiard-Triquet C (2007) Biomonitoring in a clean and a multi-contaminated estuary based on biomarkers and chemical analyses in the endobenthic worm Nereis diversicolor. Environ Pollut 148(2):445–458. https://doi.org/10.1016/j.envpol.2006.12.022
El Zrelli R, Courjault-Radé P, Rabaoui L, Castet S, Michel S, Bejaoui N (2015) Heavy metal contamination and ecological risk assessment in the surface sediments of the coastal area surrounding the industrial complex of Gabes city, Gulf of Gabes, SE Tunisia. Mar Pollut Bull 101(2):922–929. https://doi.org/10.1016/j.marpolbul.2015.10.047
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Ferreira M, Moradas-Ferreira P, Reis-Henriques MA (2005) Oxidative stress biomarkers in two resident species, mullet (Mugil cephalus) and flounder (Platichthys flesus), from a polluted site in River Douro Estuary, Portugal. Aquat Toxicol 71(1):39–48. https://doi.org/10.1016/j.aquatox.2004.10.009
Flohé L (1989) Structure and catalytic mechanism of glutathione peroxidase. In: Taniguchi N, Higashi T, Sakamoto Y, Meister A (eds) Glutathione centennial: molecular perspectives and clinical implications. Academic Press, London, p 103–114
Geracitano LA, Bocchetti R, Monserrat JM, Regoli F, Bianchini A (2004) Oxidative stress responses in two populations of Laeonereis acuta (Polychaeta, Nereididae) after acute and chronic exposure to copper. Mar Environ Res 58(1):1–17. https://doi.org/10.1016/j.marenvres.2003.09.001
Ghedira J, Jebali J, Bouraoui Z, Banni M, Chouba L, Boussetta H (2009) Acute effects of chlorpyryphos-ethyl and secondary treated effluents on acetylcholinesterase and butyrylcholinesterase activities in Carcinus maenas. J Environ Sci 21(10):1467–1472. https://doi.org/10.1016/S1001-0742(08)62441-9
Ghedira J, Jebali J, Banni M, Chouba L, Boussetta H, López-Barea J, Alhama J (2011) Use of oxidative stress biomarkers in Carcinus maenas to assess littoral zone contamination in Tunisia. Aquat Biol 14(1):87–98. https://doi.org/10.3354/ab00377
Gonçalves C, Teixeira C, Basto MCP, Almeida CMR (2016) PAHs levels in Portuguese estuaries and lagoons: salt marsh plants as potential agents for the containment of PAHs contamination in sediments. Reg Stud Mar Sci 7:211–221. https://doi.org/10.1016/j.rsma.2016.05.004
Greco L, Serrano R, Blanes MA, Serrano E, Capri E (2010) Bioaccumulation markers and biochemical responses in European sea bass (Dicentrarchus labrax) raised under different environmental conditions. Ecotoxicol Environ Saf 73(1):38–45. https://doi.org/10.1016/j.ecoenv.2009.09.011
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-Transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139
Hageman JJ, Bast A, Vermeulen NPE (1992) Monitoring of oxidative free radical damage in vivo: analytical aspects. Chemico-Biol Interact 82(3):243–293. https://doi.org/10.1016/0009-2797(92)90001-2
Hansen BH, Rømma S, Garmo ØA, Pedersen SA, Olsvik PA, Andersen RA (2007) Induction and activity of oxidative stress-related proteins during waterborne Cd/Zn-exposure in brown trout (Salmo trutta). Chemosphere 67(11):2241–2249. https://doi.org/10.1016/j.chemosphere.2006.12.048
Janssens BJ, Childress JJ, Baguet F, Rees J-F (2000) Reduced enzymatic antioxidative defense in deep-sea fish. J Exp Biol 203(24):3717–3725
Jebali J, Banni M, Guerbej H, Almeida EA, Bannaoui A, Boussetta H (2006) Effects of malathion and cadmium on acetylcholinesterase activity and metallothionein levels in the fish Seriola dumerilli. Fish Physiol Biochem 32(1):93–98. https://doi.org/10.1007/s10695-006-0041-2
Jelassi R, Khemaissia H, Zimmer M, Garbe-Schönberg D, Nasri-Ammar K (2015) Biodiversity of talitridae family (Crustacea, Amphipoda) in some Tunisian coastal lagoons. Zool Stud 54(1):17. https://doi.org/10.1186/s40555-014-0096-1
Kalman J, Palais F, Amiard JC, Mouneyrac C, Muntz A, Blasco J, Riba I, Amiard-Triquet C (2009) Assessment of the health status of populations of the ragworm Nereis diversicolor using biomarkers at different levels of biological organisation. Mar Ecol Prog Ser 393:55–67. https://doi.org/10.3354/meps08239
Kalman J, Buffet PE, Amiard JC, Denis F, Mouneyrac C, Amiard-Triquet C (2010) Assessment of the influence of confounding factors (weight, salinity) on the response of biomarkers in the estuarine polychaete Nereis diversicolor. Biomarkers 15(5):461–469. https://doi.org/10.3109/1354750X.2010.491162
Kharroubi A, Gzam M, Jedoui Y (2012) Anthropogenic and natural effects on the water and sediments qualities of costal lagoons: case of the Boughrara Lagoon (Southeast Tunisia). Environ Earth Sci 67(4):1061–1067. https://doi.org/10.1007/s12665-012-1551-0
Lionetto F, Del Sole R, Cannoletta D, Vasapollo G, Maffezzoli A (2012) Monitoring wood degradation during weathering by cellulose crystallinity. Materials 5(10):1910–1922. https://doi.org/10.3390/ma5101910
Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42(8):656–666. https://doi.org/10.1016/S0025-326X(01)00060-1
Livingstone DR, Lemaire P, Matthews A, Peters L, Bucke D, Law RJ (1993) Pro-oxidant, antioxidant and 7-ethoxyresorufin O-deethylase (EROD) activity responses in liver of dab (Limanda limanda) exposed to sediment contaminated with hydrocarbons and other chemicals. Mar Pollut Bull 26(11):602–606. https://doi.org/10.1016/0025-326X(93)90498-9
Louati A, Elleuch B, Kallel M, Saliot A, Dagaut J, Oudot J (2001) Hydrocarbon contamination of coastal sediments from the Sfax area (Tunisia), Mediterranean Sea. Mar Pollut Bull 42(6):444–451. https://doi.org/10.1016/S0025-326X(00)00179-X
Lubos E, Loscalzo J, Handy DE (2011) Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 15(7):1957–1997. https://doi.org/10.1089/ars.2010.3586
Lucan-Bouché ML, Biagianti-Risbourg S, Arsac F, Vernet G (1999) An original decontamination process developed by the aquatic oligochaete Tubifex exposed to copper and lead. Aquat Toxicol 45(1):9–17. https://doi.org/10.1016/S0166-445X(98)00091-5
Maranho LA, Baena-Nogueras RM, Lara-Martín PA, Del Valls TA, Martín-Díaz ML (2014) Bioavailability, oxidative stress, neurotoxicity and genotoxicity of pharmaceuticals bound to marine sediments. The use of the polychaete Hediste diversicolor as bioindicator species. Environ Res 134:353–365. https://doi.org/10.1016/j.envres.2014.08.014
Matthiessen P, Law RJ (2002) Contaminants and their effects on estuarine and coastal organisms in the United Kingdom in the late twentieth century. Environ Pollut 120(3):739–757. https://doi.org/10.1016/S0269-7491(02)00175-6
Moreira SM, Moreira-Santos M, Guilhermino L, Ribeiro R (2005) A short-term sub-lethal in situ toxicity assay with Hediste diversicolor (polychaeta) for estuarine sediments based on post exposure feeding. Environ Toxicol Chem 24(8):2010–2018. https://doi.org/10.1897/04-473R1.1
Moreira SM, Lima I, Ribeiro R, Guilhermino L (2006) Effects of estuarine sediment contamination on feeding and on key physiological functions of the polychaete Hediste diversicolor: laboratory and in situ assays. Aquatic Toxicol 78(2):186–201. https://doi.org/10.1016/j.aquatox.2006.03.001
Mseddi S, Chaari L, Belaid C, Chakchouk I, Kallel M (2016) Valorization of treated olive mill wastewater in fertigation practice. Environ Sci Pollut Res 23(16):15792–15800. https://doi.org/10.1007/s11356-015-4353-6
Mucha AP, Bordalo AA, Vasconcelos MT (2010) Anthropogenic impact on the benthic dynamics in the Douro estuary—an integrated assessment. Situation and Perspectives for the European Union, 6–10 May 2010 Porto
Nunes B, Vidal D, Barbosa I, Soares AMVM, Freitas R (2016) Pollution effects on biochemical pathways determined in the polychaete Hediste diversicolor collected in three Portuguese estuaries. Environ Sci Processes Impacts 18(9):1208–1219. https://doi.org/10.1039/C6EM00297H
Oliva M, González de Canales ML, Gravato C, Guilhermino L, Perales JA (2010) Biochemical effects and polycyclic aromatic hydrocarbons (PAHs) in Senegal sole (Solea senegalensis) from a Huelva estuary (SW Spain). Ecotoxicol Environ Saf 73(8):1842–1851. https://doi.org/10.1016/j.ecoenv.2010.08.035
Oliva M, José Vicente J, Gravato C, Guilhermino L, Dolores Galindo-Riaño M (2012) Oxidative stress biomarkers in Senegal sole, Solea senegalensis, to assess the impact of heavy metal pollution in a Huelva estuary (SW Spain): seasonal and spatial variation. Ecotoxicol Environ Saf 75(1):151–162. https://doi.org/10.1016/j.ecoenv.2011.08.017
Peña-Llopis S, Ferrando MD, Peña JB (2003) Fish tolerance to organophosphate-induced oxidative stress is dependent on the glutathione metabolism and enhanced by N-acetylcysteine. Aquat Toxicol 65(4):337–360. https://doi.org/10.1016/S0166-445X(03)00148-6
Pergent G, Zaouali J (1992) Analyse phénologique et lépidochronologique de Posidonia oceanica dans une lagune hyperhaline du Sud Tunisien. In: Rapport de la Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranee, vol 33, pp 48–49
Rabaoui L, Balti R, Zrelli R, Tlig-Zouari S (2014) Assessment of heavy metals pollution in the gulf of Gabes (Tunisia) using four mollusk species. Mediterr Mar Sci 15(1):45–58. https://doi.org/10.12681/mms.504
Rajkumar J (2011) Biochemical markers of oxidative stress in Mugil cephalus exposed to cadmium, copper, lead and zinc. Int J Pharma Bio Sci 2(3):41–50
Reis PA, Antunes JC, Almeida CMR (2009) Metal levels in sediments from the Minho estuary salt marsh: a metal clean area? Environ Monitor Assess 159(1–4):191. https://doi.org/10.1007/s10661-008-0622-x
Rekik A, Denis M, Dugenne M, Barani A, Maalej S, Ayadi H (2014) Seasonal distribution of ultra phytoplankton and heterotrophic prokaryotes in relation to abiotic variables on the north coast of Sfax after restoration. Mar Pollut Bull 84(1–2):280–305. https://doi.org/10.1016/j.marpolbul.2014.05.003
Rice-Evans C, Diplock AT, Symons MC (1991) Techniques in free radical research. Sole distributors for the USA and Canada. Elsevier, Amsterdam. https://doi.org/10.1016/0014-5793(92)81064-S
Romeo M, Bennani N, Gnassia-Barelli M, Lafaurie M, Girard JP (2000) Cadmium and copper display different responses towards oxidative stress in the kidney of the sea bass Dicentrarchus labrax. Aquat Toxicol 48(2–3):185–194. https://doi.org/10.1016/S0166-445X(99)00039-9
Ruilian YU, Xing Y, Ruiliananhui Z, Gongren HU, Xianglin TU (2008) Heavy metal pollution in intertidal sediments from Quanzhou Bay, China. J Environ Sci 20(6):664–669. https://doi.org/10.1016/S1001-0742(08)62110-5
Saliot A (2004) Évolution de la pollution de l’océan mondial et de la Méditerranée par les hydrocarbures sur les quarante dernières années (1960–2000). Oceanis 30(4):449–459
Scaps P (2002) A review of the biology, ecology and potential use of the common ragworm Hediste diversicolor (OF Müller) (Annelida: Polychaeta). Hydrobiologia 470(1–3):203–218. https://doi.org/10.1023/A:1015681605656
Scaps P, Demuynck S, Descamps M, Dhainaut A (1996) Biochemical and enzymatic characterization of an acetylcholinesterase from Nereis diversicolor (Annelida, Polychaeta): comparison with the cholinesterases of Eisenia fetida (Annelida, Oligochaeta). Biol Bull 190(3):396–402. https://doi.org/10.2307/1543032
SFT (2007) Guidelines for classification of environmental quality in fjords and coastal areas. Revision of classification of metals and organic contaminants in water and sediment. Norwegian Statens ForurensningsTilsyn (SFT), Norwegian Pollution Control Authority SFT TA-2229/2007
Shepard FP (1954) Nomenclature based on sand-silt-clay ratios SEPM. J Sediment Res, vol 24. http://dx.doi.org/10.1306/D4269774-2B26-11D7-8648000102C1865D
Solé M, Kopecka-Pilarczyk J, Blasco J (2009) Pollution biomarkers in two estuarine invertebrates, Nereis diversicolor and Scrobicularia plana, from a Marsh ecosystem in SW Spain. Environ Int 35(3):523–531. https://doi.org/10.1016/j.envint.2008.09.013
Sun FH, Zhou QX (2008) Oxidative stress biomarkers of the polychaete Nereis diversicolor exposed to cadmium and petroleum hydrocarbons. Ecotoxicol Environ Saf 70(1):106–114. https://doi.org/10.1016/j.ecoenv.2007.04.014
Tlili S, Métais I, Boussetta H, Mouneyrac C (2010) Linking changes at sub-individual and population levels in Donax trunculus: assessment of marine stress. Chemosphere 81(6):692–700. https://doi.org/10.1016/j.chemosphere.2010.07.064
Van der Oost R, Goksøyr A, Celander M, Heida H, Vermeulen NPE (1996) Biomonitoring of aquatic pollution with feral eel (Anguilla anguilla) II biomarkers: pollution-induced biochemical responses. Aquat Toxicol 36(3–4):189–222. https://doi.org/10.1016/S0166-445X(96)00802-8
Van der Oost R, Lopes SCC, Komen H, Satumalay K, den Bos R, Heida H, Vermeulen NPE (1998) Assessment of environmental quality and inland water pollution using biomarker responses in caged carp (Cyprinus carpio): use of a bioactivation: detoxication ratio as a biotransformation index (BTI). Mar Environ Res 46(1–5):315–319. https://doi.org/10.1016/S0141-1136(97)00096-2
Van der Oost D, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149. https://doi.org/10.1016/S1382-6689(02)00126-6
Van Veld PA, Sanders BM, Fowler BA, Lars F, Di Giulio RT, Marius B, Stegeman JJ (2018) Molecular responses to environmental contamination: enzyme and protein systems as indicators of chemical exposure and effect. Biomarkers. CRC Press, Boca Raton, pp 235–336
Vieira LR, Sousa A, Frasco MF, Lima I, Morgado F, Guilhermino L (2008) Acute effects of benzo[a]pyrene, anthracene and a fuel oil on biomarkers of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Sci Total Environ 395(2–3):87–100. https://doi.org/10.1016/j.scitotenv.2008.01.052
Vieira C, Morais S, Ramos S, Delerue-Matos C, Oliveira MBPP (2011) Mercury, cadmium, lead and arsenic levels in three pelagic fish species from the Atlantic Ocean: intra- and inter-specific variability and human health risks for consumption. Food Chem Toxicol 49(4):923–932. https://doi.org/10.1016/j.fct.2010.12.016
Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils-Effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63(4):251–264
Wang Y, Yang L, Kong L, Liu E, Wang L, Zhu J (2015) Spatial distribution, ecological risk assessment and source identification for heavy metals in surface sediments from Dongping Lake, Shandong, East China. Catena 125:200–205. https://doi.org/10.1016/j.catena.2014.10.023
Yuan X, Chen A, Zhou Y, Liu H, Yang D (2010) The influence of cadmium on the antioxidant enzyme activities in polychaete Perinereis aibuhitensis Grube (Annelida: Polychaeta). Chin J Oceanol Limnol 28(4):849–855. https://doi.org/10.1007/s00343-010-9127-x
Zaghden H, Kallel M, Louati A, Elleuch B, Oudot J, Saliot A (2005) Hydrocarbons in surface sediments from the Sfax coastal zone, (Tunisia). Mediterr Sea Mar Pollut Bull 50(11):1287–1294. https://doi.org/10.1016/j.marpolbul.2005.04.045
Zaghden H, Kallel M, Elleuch B, Oudot J, Saliot A, Sayadi S (2014) Evaluation of hydrocarbon pollution in marine sediments of Sfax coastal areas from the Gabes Gulf of Tunisia, Mediterranean Sea. Environ Earth Sci 72(4):1073–1082. https://doi.org/10.1007/s12665-013-3023-6
Zaghden H, Serbaji MM, Saliot A, Sayadi S (2016) The Tunisian Mediterranean coastline: potential threats from urban discharges Sfax-Tunisian Mediterranean coasts. Desalin Water Treat 57(52):24765–24777. https://doi.org/10.1080/19443994.2016.1149107
Acknowledgements
The authors are grateful to the “Erasmus Mundus Programme” for providing scholarship to R. Ghribi through the “Battuta” program (Building Academic Ties towards Universities through Training Activities) dedicated to the development of relations between Europe and North Africa through grants of excellence between the two regions. The authors are grateful to the Tunisian Ministry of Higher Education and Scientific Research also supported this thesis. This work was conducted in the framework of Researcher FCT Program (Operational Program for Human Potential, QREN, EU) who hired Bruno Nunes. The authors are particularly thankful to Prof. Abdelmajid Dammak for his contribution to correct grammatical errors and to improve the English writing skills of this paper. This research was also supported by the European Regional Development Fund (ERDF) through the COMPETE—Operational Competitiveness Program and by national funds through FCT—Foundation for Science and Technology, under the projects “PEst-C/MAR/LA0015/2013” and “UID/Multi/04423/2013” in the framework of the programme PT2020.
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Ghribi, R., Correia, A.T., Elleuch, B. et al. Toxicity Assessment of Impacted Sediments from Southeast Coast of Tunisia Using a Biomarker Approach with the Polychaete Hediste diversicolor. Arch Environ Contam Toxicol 76, 678–691 (2019). https://doi.org/10.1007/s00244-019-00611-2
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DOI: https://doi.org/10.1007/s00244-019-00611-2