Abstract
In the present study, a multi-biomarker approach was used to assess the biological effects of metal pollution in the southern lagoon of Tunis, on clam Ruditapes decussatus both in “hot” (in summer) and “cold” (in winter) seasons. Clams were collected in August 2015 and February 2016 from three sites of the lagoon and from Louza considered a reference site. The concentrations of five trace metals (cadmium, copper, iron, lead, and zinc) in the soft tissues of R. decussatus were evaluated at the sampling sites. A core of biomarkers indicative of (a) neurotoxicity (acetylcholinesterase, AChE); (b) biotransformation (glutathione S-transferase, GST); (c) oxidative stress (catalase, CAT; total glutathione peroxidase, T-GPx; total glutathione peroxidase, T-GPx; selenium-dependent glutathione peroxidase, Se-GPx; glutathione reductase, GR; superoxide dismutase, SOD) (d) lipid peroxidation (malondialdhyde, MDA level), and (e) apoptotic process (caspase 3-like, CSP3) was selected for measurements of environmental effects on the populations of clams collected from the different sampling sites. The results of metal bioaccumulation in soft tissues of Ruditapes decussatus revealed a high pollution in the South Lagoon of Tunis with spatial variation and relatively high levels at the navigation channel. Anthropogenic pollutants in the lagoon led to the activation of antioxidant defense and biotransformation enzymes to oxidative damage of the membrane and activation of apoptosis, and revealed neurotoxicity. Among this core of biomarkers, the antioxidants enzymes (CAT, SOD, GR, and GPx) were very sensitive, allowing the discrimination among sites and pointing to the navigation channel as the most impacted site in the southern lagoon of Tunis. Moreover, a significant effect of season was recorded on biomarkers responses (e.g., CAT, GR, SOD, AChE, and CSP3 activities and MDA levels) with higher levels in winter than in summer, probably influenced by the reproductive stage and food availability. Finally, the measurement of the selected core of biomarkers in the whole soft tissues of clams was considered as an integrated indicator of environmental stress. Moreover, R. decussatus proved to be a remarkable sentinel species capable to establish a reliable diagnosis of the health status of the marine environment in different areas of the southern lagoon of Tunis, both in “hot” and “cold” seasons.
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References
Aebi H (1984) [13] Catalase in vitro. Methods Enzymol 105:121–126
Ahamed M, Posgai R, Gorey TJ, Nielsen M, Hussain SM, Rowe JJ (2010) Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol 242:263–269
Ahmad I, Coelho JP, Mohmood I, Pacheco M, Santos MA, Duarte AC, Pereira E (2011) Immunosuppression in the infaunal bivalve Scrobicularia plana environmentally exposed to mercury and association with its accumulation. Chemosphere 82:1541–1546
Akcha F, Izuel C, Venier P, Budzinski H, Burgeot T, Narbonne J (2000) Enzymatic biomarker measurement and study of DNA adduct formation in benzo [a] pyrene-contaminated mussels, Mytilus galloprovincialis. Aquat Toxicol 49:269–287
An MI, Choi CY (2010) Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. Comp Biochem Physiol B Biochem Mol Biol 155:34–42
Andrade M, De Marchi L, Soares AMVM, Rocha RJM, Figueira E, Freitas R (2019) Are the effects induced by increased temperature enhanced in Mytilus galloprovincialis submitted to air exposure? Sci Total Environ 647:431–440
Angilletta M, Sears M (2000) The metabolic cost of reproduction in an oviparous lizard. Funct Ecol 14:39–45
Attig H, Kamel N, Sforzini S, Dagnino A, Jamel J, Boussetta H, Viarengo A, Banni M (2014) Effects of thermal stress and nickel exposure on biomarkers responses in Mytilus galloprovincialis (Lam). Mar Environ Res 94:65–71
Banni M, Rym B, Amor E, Hamadi B (2003) Genotoxicity, catalase, and acetylcholinesterase in the assessment of the pollution status of some sites on the Tunisian littoral. Bull Environ Contam Toxicol 70:0854–0860
Banni M, Jebali J, Daubeze M, Clerandau C, Guerbej H, Narbonne J, Boussetta H (2005) Monitoring pollution in Tunisian coasts: application of a classification scale based on biochemical markers. Biomarkers 10:105–116
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
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
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
Bebianno MJ, Serafim MA (2003) Variation of metal and metallothionein concentrations in a natural population of Ruditapes decussatus. Arch Environ Contam Toxicol 44:53–66
Bebianno M, Geret F, Hoarau P, Serafim M, Coelho M, Gnassia-Barelli M, Romeo M (2004) Biomarkers in Ruditapes decussatus: a potential bioindicator species. Biomarkers 9:305–330
Béguel JP, Huvet A, Quillien V, Lambert C, Fabioux C (2013) Study of the antioxidant capacity in gills of the Pacific oyster Crassostrea gigas in link with its reproductive investment. Comp Biochem Physiol C Toxicol Pharmacol 157:63–71
Bocchetti R, Regoli F (2006) Seasonal variability of oxidative biomarkers, lysosomal parameters, metallothioneins and peroxisomal enzymes in the Mediterranean mussel Mytilus galloprovincialis from Adriatic Sea. Chemosphere 65:913–921
Borković SS, Pavlović SZ, Kovačević TB, Štajn AŠ, Petrović VM, Saičić ZS (2008) Antioxidant defence enzyme activities in hepatopancreas, gills and muscle of Spiny cheek crayfish (Orconectes limosus) from the River Danube. Comp Biochem Physiol C Toxicol Pharmacol 147:122–128
Boukadida K, Cachot J, Clérandeaux C, Gourves P-Y, Banni M (2017) Early and efficient induction of antioxidant defense system in Mytilus galloprovincialis embryos exposed to metals and heat stress. Ecotoxicol Environ Saf 138:105–112
Boutet I, Tanguy A, Moraga D (2004) Response of the Pacific oyster Crassostrea gigas to hydrocarbon contamination under experimental conditions. Gene 329:147–157
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 72:248–254
Breitwieser M, Viricel A, Graber M, Murillo L, Becquet V, Churlaud C, Fruitier-Arnaudin I, Huet V, Lacroix C, Pante E (2016) Short-term and long-term biological effects of chronic chemical contamination on natural populations of a marine bivalve. PLoS ONE 11:150–184
Buege JA, Aust SD (1978) [30] Microsomal lipid peroxidation. Methods Enzymol 52:302–310
Buffet PE, Pan JF, Poirier L, Amiard-Triquet C, Amiard JC, Gaudin P, Risso-de Faverney C, Guibbolini M, Gilliland D, Valsami-Jones E (2013) Biochemical and behavioural responses of the endobenthic bivalve Scrobicularia plana to silver nanoparticles in seawater and microalgal food. Ecotoxicol Environ Saf 89:117–124
Buffet PE, Zalouk-Vergnoux A, Châtel A, Berthet B, Métais I, Perrein-Ettajani H, Poirier L, Luna-Acosta A, Thomas-Guyon H, Risso-de Faverney C (2014) A marine mesocosm study on the environmental fate of silver nanoparticles and toxicity effects on two endobenthic species: the ragworm Hediste diversicolor and the bivalve mollusc Scrobicularia plana. Sci Total Environ 470:1151–1159
Cajaraville MP, Bebianno MJ, 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
Campillo JA, Albentosa M, Valdés NJ, Moreno-González R, León VM (2013) Impact assessment of agricultural inputs into a Mediterranean coastal lagoon (Mar Menor, SE Spain) on transplanted clams (Ruditapes decussatus) by biochemical and physiological responses. Aquat Toxicol 142:365–379
Camus L, Jones M, Børseth J, Grøsvik B, Regoli F, Depledge M (2002) Total oxyradical scavenging capacity and cell membrane stability of haemocytes of the Arctic scallop, Chlamys islandicus, following benzo (a) pyrene exposure. Mar Environ Res 54:425–430
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
Chakraborty S, Ray M, Ray S (2013) Cell to organ: physiological, immunotoxic and oxidative stress responses of Lamellidens marginalis to inorganic arsenite. Ecotoxicol Environ Saf 94:153–163
Chalghmi H, Bourdineaud JP, 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
Chalghmi H, Zrafi I, Gourves PY, 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 Impact 18:895–907
Charrada RB (1992) Le lac de Tunis après les aménagements. Paramètres physico-chimiques de l’eau et relation avec la croissance des macroalgues. Mar Life 1:29–44
Clairbone A (1985) Catalase activity. In: Greenwald RA (ed) CRC handbook of methods in oxygen radical research. CRC Press, Boca Raton
Coles JA, Farley SR, Pipe RK (1994) Effects of fluoranthene on the immunocompetence of the common marine mussel, Mytilus edulis. Aquat Toxicol 30:367–379
Cravo A, Pereira C, Gomes T, Cardoso C, Serafim A, Almeida C, Rocha T, Lopes B, Company R, Medeiros A (2012) A multibiomarker approach in the clam Ruditapes decussatus to assess the impact of pollution in the Ria Formosa lagoon, South Coast of Portugal. Mar Environ Res 75:23–34
Cravo A, Lopes B, Serafim A, Company R, Barreira L, Gomes T, Bebianno MJ (2013) Spatial and seasonal biomarker responses in the clam Ruditapes decussatus. Biomarkers 18:30–43
Dabrowska H, Kopko O, Turja R, Lehtonen KK, Góra A, Polak-Juszczak L, Warzocha J, Kholodkevich S (2013) Sediment contaminants and contaminant levels and biomarkers in caged mussels (Mytilus trossulus) in the southern Baltic Sea. Mar Environ Res 84:1–9
de Lafontaine Y, Gagné F, Blaise C, Costan G, Gagnon P, Chan H (2000) Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada). Aquat Toxicol 50:51–71
De Luca-Abbott SB, Richardson BJ, McClellan KE, Zheng GJ, Martin M, Lam PK (2005) Field validation of antioxidant enzyme biomarkers in mussels (Perna viridis) and clams (Ruditapes philippinarum) transplanted in Hong Kong coastal waters. Mar Pollut Bull 51:694–707
de Oliveira LF, Cabral MT, Risso WE, dos Reis Martinez CB (2018) Single and combined effects of Zn, Mn and Fe on the Neotropical freshwater bivalve Anodontites trapesialis: bioaccumulation and biochemical biomarkers. Ecotoxicol Environ Saf 161:735–745
Dellali M, Romeo M, Gnassia-Barelli M, Aïssa P (2004) A multivariate data analysis of the clam Ruditapes decussatus as sentinel organism of the Bizerta lagoon (Tunisia). Water Air Soil Poll 156:131–144
Depledge M (1994) The rational basis for the use of biomarkers as ecotoxicological tools. Nondestruct Biomark Vertebr 1994:271–295
Dyrynda EA, Pipe RK, Burt GR, Ratcliffe NA (1998) Modulations in the immune defences of mussels (Mytilus edulis) from contaminated sites in the UK. Aquat Toxicol 42:169–185
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88
Fernández B, Campillo J, Martínez-Gómez C, Benedicto J (2010) Antioxidant responses in gills of mussel (Mytilus galloprovincialis) as biomarkers of environmental stress along the Spanish Mediterranean coast. Aquat Toxicol 99:186–197
Fournier M, Pellerin J, Lebeuf M, Brousseau P, Morin Y, Cyr D (2002) Effects of exposure of Mya arenaria and Mactromeris polynyma to contaminated marine sediments on phagocytic activity of hemocytes. Aquat Toxicol 59:83–92
Galgani F, Bocquene G (1991) Semi-automated colorimetric and enzymatic assays for aquatic organisms using microplate readers. Water Res 25:147–150
Galgani F, Bocquené G (2000) Molecular biomarkers of exposure of marine organisms to organophosphorus pesticides and carbamates. Use of biomarkers for environmental quality assessment. Elsevier Science Publisher, Amsterdam
González-Fernández C, Albentosa M, Campillo JA, Viñas L, Franco A, Bellas J (2016) Effect of mussel reproductive status on biomarker responses to PAHs: implications for large-scale monitoring programs. Aquat Toxicol 177:380–394
Grütter MG (2000) Caspases: key players in programmed cell death. Curr Opin Struct Biol 10:649–655
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Halliwell B, Gutteridge JMC (1986) Oxygen free radicals and iron in relation to biology and medicine: some problems and concepts. Arch Biochem Biophys 246:501–514
Hamida L, Medhiouband M, Cochard J-C, Romdhane M, Le Pennec M (2004) Étude comparative du cycle de reproduction de la palourde Ruditapes decussatus en milieu naturel (sud Tunisie) et contrôlé (écloserie). Cah Biol Mar 45:291–303
Harbridge W, Pilkey OH, Whaling P, Swetland P (1976) Sedimentation in the Lake of Tunis: a lagoon strongly influenced by man. Environ Geol 1:215–225
Hellal MEA, Hellal F, El Khemissi Z, Jebali R, Dachraoui M (2011) Trace metals in algae and sediments from the north-eastern Tunisian lagoons. Bull Environ Cont Toxicol 86:194–198
Hoarau P, Gnassia-Barelli M, Romeo M, Girard JP (2001) Differential induction of glutathione S-transferases in the clam Ruditapes decussatus exposed to organic compounds. Environ Toxicol Chem 20:523–529
Hoarau P, Garello G, Gnassia-Barelli M, Roméo M, Girard J-P (2004) Effect of three xenobiotic compounds on glutathione S-transferase in the clam Ruditapes decussatus. Aquat Toxicol 68:87–94
Höher N, Köhler A, Strand J, Broeg K (2012) Effects of various pollutant mixtures on immune responses of the blue mussel (Mytilus edulis) collected at a salinity gradient in Danish coastal waters. Mar Environ Res 75:35–44
Hong WJ, Jia H, Li YF, Sun Y, Liu X, Wang L (2016) Polycyclic aromatic hydrocarbons (PAHs) and alkylated PAHs in the coastal seawater, surface sediment and oyster from Dalian, Northeast China. Ecotoxicol Environ Saf 128:11–20
Hu M, Li L, Sui Y, Li J, Wang Y, Lu W, Dupont S (2015) Effect of pH and temperature on antioxidant responses of the thick shell mussel Mytilus coruscus. Fish Shellfish Immunol 46:573–583
IPCC Cctpsb (2007) In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 96
Jiang W, Fang J, Gao Y, Du M, Fang J, Wang X, Li F, Lin F, Jiang Z (2019) Biomarkers responses in Manila clam, Ruditapes philippinarum after single and combined exposure to mercury and benzo [a] pyrene. Comp Biochem Physiol C Toxicol Pharmacol 220:1–8
Jouini Z, Charrada RB, Moussa M (2005) Caractéristiques du Lac Sud de Tunis après sa restauration. Mar Life 15:3–11
Kiss T (2010) Apoptosis and its functional significance in molluscs. Apoptosis 15:313–321
Lau P, Wong H, Garrigues P (2004) Seasonal variation in antioxidative responses and acetylcholinesterase activity in Perna viridis in eastern oceanic and western estuarine waters of Hong Kong. Cont Shelf Res 24:1969–1987
Lawen A (2003) Apoptosis—an introduction. BioEssays 25:888–896
Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952–958
Lin T, Zhou K, Lai Q, Yao Z, Li Z, Xing J (2012) Seasonal variations of water temperature, food availability, size, and reproduction on the hemocyte parameters in the scallop Chlamys farreri. J Shellfish Res 31:663–670
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30
Manduzio H, Monsinjon T, Galap C, Leboulenger F, Rocher B (2004) Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquat Toxicol 70:83–93
Maranho L, André C, DelValls T, Gagné F, Martín-Díaz M (2015) In situ evaluation of wastewater discharges and the bioavailability of contaminants to marine biota. Sci Total Environ 538:876–887
Marques A, Piló D, Carvalho S, Araújo O, Guilherme S, Santos MA, Vale C, Pereira F, Pacheco M, Pereira P (2018) Metal bioaccumulation and oxidative stress profiles in Ruditapes philippinarum–insights towards its suitability as bioindicator of estuarine metal contamination. Ecol Indic 95:1087–1099
Matias D, Joaquim S, Matias AM, Moura P, de Sousa JT, Sobral P, Leitão A (2013) The reproductive cycle of the European clam Ruditapes decussatus (L., 1758) in two Portuguese populations: implications for management and aquaculture programs. Aquaculture 406:52–61
Matozzo V, Binelli A, Parolini M, Locatello L, Marin MG (2010) Biomarker responses and contamination levels in the clam Ruditapes philippinarum for biomonitoring the Lagoon of Venice (Italy). J Environ Monit 12:776–786
Matozzo V, Binelli A, Parolini M, Previato M, Masiero L, Finos L, Bressan M, Marin MG (2012) Biomarker responses in the clam Ruditapes philippinarum and contamination levels in sediments from seaward and landward sites in the Lagoon of Venice. Ecol Indic 19:191–205
McCord JM, Fridovich I (1969) Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6049–6055
Monserrat JM, Martínez PE, Geracitano LA, Amado LL, Martins CMG, Pinho GLL, Chaves IS, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol C Toxicol Pharmacol 146:221–234
Mzoughi N, Chouba L (2011) Distribution of trace metals, aliphatic hydrocarbons and polycyclic aromatic hydrocarbons in sediment cores from the Sicily Channel and the Gulf of Tunis (southwestern Mediterranean Sea). Environ Technol 32:43–54
Nasci C, Da Ros L, Campesan G, Van Vleet ES, Salizzato M, Sperni L, Pavoni B (1999) Clam transplantation and stress-related biomarkers as useful tools for assessing water quality in coastal environments. Mar Pollut Bull 39:255–260
Opferman JT, Korsmeyer SJ (2003) Apoptosis in the development and maintenance of the immune system. Nat Immunol 4:410–415
Palais F, Dedourge-Geffard O, Beaudon A, Pain-Devin S, Trapp J, Geffard O, Noury P, Gourlay-Francé C, Uher E, Mouneyrac C (2012) One-year monitoring of core biomarker and digestive enzyme responses in transplanted zebra mussels (Dreissena polymorpha). Ecotoxicology 21:888–905
Pampanin D, Viarengo A, Garrigues P, Andersen O (2006) Background for the beep stavanger workshops: biological effects on marine organisms in two common, large, laboratory experiments and in a field study. Comparison of the value (sensitivity, specificity, etc.) of core and new biomarkers. Aquat Toxicol 78:S1–S4
Perez T, Sartoretto S, Soltan D, Capo S, Fourt M, Dutrieux E, Vacelet J, Harmelin JG, Rebouillon P (2000) Etude bibliographique sur les bioindicateurs de l’état du milieu marin: système d’évaluation de la qualité des milieux littoraux-volet biologique [SEQ littoral-Volet bio]. Agences de l’eau, 4 fascicules
Piva F, Ciaprini F, Onorati F, Benedetti M, Fattorini D, Ausili A, Regoli F (2011) Assessing sediment hazard through a weight of evidence approach with bioindicator organisms: a practical model to elaborate data from sediment chemistry, bioavailability, biomarkers and ecotoxicological bioassays. Chemosphere 83:475–485
Regoli F, Benedetti M, Giuliani ME (2011) Antioxidant defenses and acquisition of tolerance to chemical stress. Tolerance to environmental contaminants. CRC Press, Boca Raton, pp 153–173
Risso-de Faverney C, Devaux A, Lafaurie M, Girard J, Rahmani R (2001) Toxic effects of wastewaters collected at upstream and downstream sites of a purification station in cultures of rainbow trout hepatocytes. Arch Environ Con Tox 41:129–141
Risso-de Faverney C, Guibbolini-Sabatier ME, Francour P (2010) An ecotoxicological approach with transplanted mussels (Mytilus galloprovincialis) for assessing the impact of tyre reefs immersed along the NW Mediterranean Sea. Mar Environ Res 70:87–94
Roméo M, Hoarau P, Garello G, Gnassia-Barelli M, Girard JP (2003) Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environ Pollut 122:369–378
Sandrini-Neto L, Pereira L, Martins CC, de Assis HCS, Camus L, Lana PC (2016) Antioxidant responses in estuarine invertebrates exposed to repeated oil spills: effects of frequency and dosage in a field manipulative experiment. Aquat Toxicol 177:237–249
Serdar S, Lök A (2009) Gametogenic cycle and biochemical composition of the transplanted carpet shell clam Tapes decussatus, Linnaeus 1758 in Sufa (Homa) Lagoon, Izmir, Turkey. Aquaculture 293:81–88
Solé M (2000) Assessment of the results of chemical analyses combined with the biological effects of organic pollution on mussels. Trends Anal Chem 19:1–9
Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol Res 29:1715–1733
Uluturhan E, Darılmaz E, Kontas A, Bilgin M, Alyuruk H, Altay O, Sevgi S (2019) Seasonal variations of multi-biomarker responses to metals and pesticides pollution in M. galloprovincialis and T. decussatus from Homa Lagoon, Eastern Aegean Sea. Mar Pollut Bull 141:176–186
Velez C, Figueira E, Soares AMVM, Freitas R (2017) Effects of seawater temperature increase on economically relevant native and introduced clam species. Mar Environ Res 123:62–70
Vlahogianni T, Valavanidis A (2007) Heavy-metal effects on lipid peroxidation and antioxidant defence enzymes in mussels Mytilus galloprovincialis. Chem Ecol 23:361–371
Winston GW, Di Giulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137–161
Wu Q, Leung JY, Tam NF, Chen S, Mai B, Zhou X, Xia L, Geng X (2014) Biological risk and pollution history of polycyclic aromatic hydrocarbons (PAHs) in Nansha mangrove, South China. Mar Pollut Bull 85:92–98
Zrafi I, Bakhrouf A, Rouabhia M, Saidane-Mosbahi D (2013) Aliphatic and aromatic biomarkers for petroleum hydrocarbon monitoring in Khniss Tunisian-Coast (Mediterranean Sea). Proc Environ Sci 18:211–220
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This study was supported by the PHC Maghreb project MAG 15MAG23.
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Mansour, C., Guibbolini, M., Rouane Hacene, O. et al. Oxidative Stress and Damage Biomarkers in Clam Ruditapes decussatus Exposed to a Polluted Site: The Reliable Biomonitoring Tools in Hot and Cold Seasons. Arch Environ Contam Toxicol 78, 478–494 (2020). https://doi.org/10.1007/s00244-020-00713-2
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DOI: https://doi.org/10.1007/s00244-020-00713-2