Skip to main content

Advertisement

SpringerLink
Log in

Testing the impact of contaminated sediments from the southeast marine coast of Tunisia on biota: a multibiomarker approach using the flatfish Solea senegalensis

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

Abstract

Coastal marine areas are highly vulnerable to the exposure to various types of stressors and impact of chemical pollution resulting from increasing anthropogenic activities, namely pollution by metals and polycyclic aromatic hydrocarbons (PAHs). To assess ecosystem quality and functions, biomarkers can provide information about the presence and adverse effects of pollutants. Accordingly, the present study was conducted to evaluate the chronic (28 days) biologic effects of putatively contaminated sediments from the Zarzis area, located in the south of the Gulf of Gabes on the Southern Tunisian coast, on the marine flatfish Solea senegalensis. Sediments were collected at three sampling sites, impacted by wastewater discharges, aquaculture activities, and industrial contamination, and then surveyed for metals (Cd, Cu, Cr, Hg, Zn, and Pb) and organic contaminants (polycyclic aromatic hydrocarbons). The quantified biomarkers involved the determination of oxidative stress, phase II metabolism, and the extent of lipid peroxidation (catalase, CAT; glutathione peroxidase activity: total and selenium-dependent, T-GPx and Se-GPx; activities of glutathione-S-transferases, GSTs; levels of lipid peroxidation, by means of the thiobarbituric acid reactive substances assay, TBARS) and neurotoxicity (activity of acetylcholinesterase, AChE). S. senegalensis exposed to potentially contaminated sediments, collected near the aquaculture facility, presented the highest values for the generality of biomarkers tested, and a significant inhibition of AChE activity. A few lesions have been also recorded in the gills and liver tissues of S. senegalensis following chronic exposure. However, the observed lesions in gills (e.g., epithelial lifting, lamellar fusion, gills hyperplasia and hypertrophy, and leukocyte infiltration) and liver (cytoplasmic vacuolation, enlargement of sinusoids, foci of necrosis, and eosinophilic bodies) were of minimal pathological importance and/or low prevalence that did not significantly affect the weighted histopathological indices. Finally, the biological responses evidenced by this flatfish can be potentially caused by metal and PAH pollution occurring in specific areas in the southeast of Tunisia. The type and extent of the observed biochemical alterations strongly suggest that the contaminated sediments from the surveyed areas could cause early adverse biological effects on exposed biota.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Alazemi BM, Lewis JW, Andrews EB (1996) Gill damage in the freshwater fish Gnathonemus petersii (family: Mormyridae) exposed to selected pollutants: an ultrastructural study. Environ Technol 17(3):225–238. https://doi.org/10.1080/09593331708616381

    Article  CAS  Google Scholar 

  • Ameur WB, El Megdiche Y, de Lapuente J, Barhoumi B, Trabelsi S, Ennaceur S, Camps L, Serret J, Ramos-López D, Gonzalez-Linares J, Touil S, Drissa MR, Borràs M (2015) Oxidative stress, genotoxicity and histopathology biomarker responses in Mugil cephalus and Dicentrarchus labrax gill exposed to persistent pollutants. A field study in the Bizerte Lagoon: Tunisia. Chemosphere 135:67–74. https://doi.org/10.1016/j.chemosphere.2015.02.050

    Article  CAS  Google Scholar 

  • Arellano JM, Storch V, Sarasquete C (1999) Histological changes and copper accumulation in liver and gills of the Senegale sole, Solea senegalensis. Ecotoxicol Environ Saf 44(1):62–72. https://doi.org/10.1006/eesa.1999.1801

    Article  CAS  Google Scholar 

  • Arellano JM, Storch V, Sarasquete C (2004) Ultrastructural and histochemical study on gills and skin of the Senegal sole, Solea senegalensis. J Appl Ichthyol 20:452–460

    Article  CAS  Google Scholar 

  • Atli G, Alptekin Ö, Tükel S, Canli M (2006) Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus. Comp Biochem Physiol C Toxicol Pharmacol 143(2):218–224. https://doi.org/10.1016/j.cbpc.2006.02.003

    Article  CAS  Google Scholar 

  • Banni M, Bouraoui Z, Ghedira J, Clerandeau C, Guerbej H, Narbonne JF, Boussetta H (2009) 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

    Article  CAS  Google Scholar 

  • Barhoumi B, Jouili S, Elbarhoumi A, Derouiche A, El Megdiche Y, Bouabdallah S, Touil S, Driss MR (2016) Organochlorines in the surface sediments of the Bahiret el Bibane lagoon (Tunisia, Southwestern Mediterranean Sea). Chem Ecol 32(9):884–897. https://doi.org/10.1080/02757540.2016.1195817

    Article  CAS  Google Scholar 

  • Basha PS, Rani AU (2003) Cadmium-induced antioxidant defense mechanism in freshwater teleost Oreochromis mossambicus (Tilapia). Ecotoxicol Environm Saf 56(2):218–221. https://doi.org/10.1016/S0147-6513(03)00028-9

    Article  CAS  Google Scholar 

  • Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: Proposal for a protocol to assess aquatic pollution. J Fish Dis 22(1):25–34. https://doi.org/10.1046/j.1365-2761.1999.00134.x

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310. https://doi.org/10.1016/S0076-6879(78)52032-6

    Article  CAS  Google Scholar 

  • Burchiel SW, Thompson TA, Lauer FT, Oprea TI (2007) Activation of dioxin response element (DRE)-associated genes by benzo (a) pyrene 3, 6-quinone and benzo (a) pyrene 1, 6-quinone in MCF-10A human mammary epithelial cells. Toxicol Appl Pharmacol 221(2):203–214. https://doi.org/10.1016/j.taap.2007.02.020

    Article  CAS  Google Scholar 

  • Camargo MMP, Martinez CBR (2007) Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotropical Ichthyol 5(3):327–336. https://doi.org/10.1590/S1679-62252007000300013

    Article  Google Scholar 

  • Cederbaum AI (2001) Introduction-serial review: alcohol, oxidative stress and cell injury. Free Radic Biol Med 31(12):1524–1526

    Article  CAS  Google Scholar 

  • Cengiz EI, Ünlü E (2003) Histopathology of gills in mosquitofish, Gambusia affinis after long-term exposure to sublethal concentrations of malathion. J Environ Sci Health B 38(5):581–589. https://doi.org/10.1081/PFC-120023516

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cinar K, Aksoy A, Emre Y, Aşti RN (2009) The histology and histochemical aspects of gills of the flower fish, Pseudophoxinus antalyae. Vet Res Commun 33(5):453. https://doi.org/10.1007/s11259-008-9191-2

    Article  Google Scholar 

  • Costa PM, Diniz MS, Caeiro S, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TA, 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(3):202–212. https://doi.org/10.1016/j.aquatox.2008.12.009

    Article  CAS  Google Scholar 

  • Costa PM, Caeiro S, Diniz MS, Lobo J, Martins M, Ferreira AM, Caetano M, Vale C, DelValls TA, Costa MH (2010) A description of chloride cell and kidney tubule alterations in the flatfish Solea senegalensis exposed to moderately contaminated estuarine sediments. J Sea Res 64:465–472

    Article  CAS  Google Scholar 

  • Crawford D, Suzuki T, Davies K (2000) Redox regulation of gene expression. Antioxidant and redox regulation of genes. Academic Press, New York, pp 21–45

    Book  Google Scholar 

  • Cutler RG (1984) Urate and ascorbate: their possible roles as antioxidants in determining longevity of mammalian species. Arch Gerontol Geriatr 3(4):321–348. https://doi.org/10.1016/0167-4943(84)90033-5

    Article  CAS  Google Scholar 

  • Delwing-de Lima D, Wollinger LF, Casagrande AC, Delwing F, da Cruz JG, Wyse AT, Delwing-Dal MD (2010) Guanidino compounds inhibit acetylcholinesterase and butyrylcholinesterase activities: effect neuroprotector of vitamins E plus C. Int J Dev Neurosci 28(6):465–473. https://doi.org/10.1016/j.ijdevneu.2010.06.008

    Article  CAS  Google Scholar 

  • Di Giulio RT, Hinton DE (2008) The toxicology of fishes. CRC Press, New York

    Book  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Esfandiari E, Shekari F, Shekari F, Esfandiari M (2007) The effect of salt stress on antioxidant enzymes’ activity and lipid peroxidation on the wheat seedling. Not Bot Horti Agrobot Cluj-Na 35(1):48

    CAS  Google Scholar 

  • Farombi EO, Adelowo OA, Ajimoko YR (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. Int J Environ Res Public Health 4(2):158–165. https://doi.org/10.3390/ijerph2007040011

    Article  CAS  Google Scholar 

  • Fernandes C, Fontaínhas-Fernandes A, Rocha E, Salgado MA (2008) Monitoring pollution in Esmoriz Paramos lagoon, Portugal: liver histological and biochemical effects in Liza saliens. Environ Monit Assess 145(1-3):315–322. https://doi.org/10.1007/s10661-007-0041-4

    Article  CAS  Google Scholar 

  • Fernández B, Campillo JA, 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(2):186–197. https://doi.org/10.1016/j.aquatox.2010.04.013

    Article  CAS  Google Scholar 

  • Fernández-Vega C, Sancho E, Ferrando MD, Andreu-Moliner E (1999) Thiobencarb toxicity and plasma AChE inhibition in the European eel. J Environ Sci Health B 34(1):61–73. https://doi.org/10.1080/03601239909373184

    Article  Google Scholar 

  • Fernández-Vega C, Sancho E, Ferrando MD, Andreu E (2002) Thiobencarb-induced changes in acetylcholinesterase activity of the fish Anguilla anguilla. Pestic Biochem Physiol 72(1):55–63. https://doi.org/10.1006/pest.2001.2581

    Article  CAS  Google Scholar 

  • Flohé L, Günzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–120. https://doi.org/10.1016/S0076-6879(84)05015-1

  • Flowers-Geary L, Bleczinski W, Harvey RG, Penning TM (1996) Cytotoxicity and mutagenicity of polycyclic aromatic hydrocarbon o-quinones produced by dihydrodiol dehydrogenase. Chem Biol Interact 99(1-3):55–72. https://doi.org/10.1016/0009-2797(95)03660-1

    Article  CAS  Google Scholar 

  • Fonseca V, Serafim Â, Bebianno MJ, Cabral H (2009) Effect of copper exposure on growth, condition indices and biomarker response in juvenile sole Solea senegalensis. Sci Mar 73:(1)51–58. https://doi.org/10.3989/scimar.2009.73n1051

  • Fonseca VF, França S, Serafim A, Company R, Lopes B, Bebianno MJ, Cabral HN (2011) Multi-biomarker responses to estuarine habitat contamination in three fish species: Dicentrarchus labrax, Solea senegalensis and Pomatoschistus microps. Aquat Toxicol 102(3-4):216–227. https://doi.org/10.1016/j.aquatox.2011.01.018

    Article  CAS  Google Scholar 

  • Fonseca VF, Vasconcelos RP, Tanner S, Franca S, Serafim A, Lopes B, Company R, Bebianno MJ, Costa MJ, Cabral HN (2015) Habitat quality of estuarine nursery grounds: Integrating non-biological indicators and multilevel biological responses in Solea senegalensis. Ecol Indic 58:335–345. https://doi.org/10.1016/j.ecolind.2015.05.064

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ghribi R, Correia AT, Elleuch B, Nunes B (2019) Toxicity assessment of impacted sediments from southeast coast of Tunisia using a biomarker approach with the polychaete Hediste diversicolor. Arch Environ Contam Toxicol 1–14. https://doi.org/10.1007/s00244-019-00611-2

  • Giari L, Manera M, Simoni E, Dezfuli BS (2007) Cellular alterations in different organs of European sea bass Dicentrarchus labrax (L.) exposed to cadmium. Chemosphere 67(6):1171–1181. https://doi.org/10.1016/j.chemosphere.2006.10.061

    Article  CAS  Google Scholar 

  • Goldberg ED, Bertine KK (2000) Beyond the mussel watch- new directions for monitoring marine pollution. Sci Total Environ 247(2-3):165–174. https://doi.org/10.1016/S0048-9697(99)00488-X

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Guicciardi ME, Malhi H, Mott JL, Gores GJ (2013) Apoptosis and necrosis in the liver. Comp Physiol 3(2):977–1010

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hajime O, Ozaki K, Yoshikawa H (2005) Identification of cytochrome P450 and glutathione-S-transferase genes preferentially expressed in chemosensory organs of the swallowtail butterfly, Papilio xuthus L. Insect Biochem Mol Biol 35(8):837–846. https://doi.org/10.1016/j.ibmb.2005.03.013

    Article  CAS  Google Scholar 

  • Hawkins WE, Overstreet RM, Provancha MJ (1984) Effects of space shuttle exhaust plumes on gills of some estuarine fishes: a light and electron microscopic study. 7(4):297–309.

  • Hermes-Lima M, Storey JM, Storey KB (2001) Antioxidant defenses and animal adaptation to oxygen availability during environmental stress. In: Cell and Molecular Response to Stress (Vol. 2, pp. 263-287). Elsevier. https://doi.org/10.1016/S1568-1254(01)80022-X

  • 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

    Article  CAS  Google Scholar 

  • Jebali J, Khedher SB, Sabbagh M, Kamel N, Banni M, Boussetta H (2013) Cholinesterase activity as biomarker of neurotoxicity: utility in the assessment of aquatic environment contamination Revista de Gestão Costeira Integrada. J Integr Coast Zone Manag 13(4). https://doi.org/10.5894/rgci430

  • Jee J-H, Kang J-C (2005) Biochemical changes of enzymatic defense system after phenanthrene exposure in olive flounder, Paralichthys olivaceus. Physiol Res 54:585–591

    CAS  Google Scholar 

  • Jena KB, Verlecar XN, Chainy GBN (2009) Application of oxidative stress indices in natural populations of Perna viridis as biomarker of environmental pollution. Mar Pollut Bull 58(1):107–113. https://doi.org/10.1016/j.marpolbul.2008.08.018

    Article  CAS  Google Scholar 

  • Jönsson ME, Brunström B, Brandt I (2009) The zebrafish gill model: Induction of CYP1A, EROD and PAH adduct formation. Aquat Toxicol 91:62–70. https://doi.org/10.1016/j.aquatox.2008.10.010

  • 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

    Article  CAS  Google Scholar 

  • Khebbeb ME, Nadji S, Amrani A (2010) The effect of cadmium exposure on malonedialdehyde and reduced glutathione concentrations in several tissues of a bivalve mollusc (Ruditapes decussatus) fished from Mellah lagoon (North East of Algeria). Ann Biol Res 1(2):166–173

    CAS  Google Scholar 

  • Köhler A, Pluta HJ (1995) Lysosomal injury and MFO activity in the liver of flounder (Platichthys flesus L.) in relation to histopathology of hepatic degeneration and carcinogenesis. Mar Environ Res 39(1-4):255–260. https://doi.org/10.1016/0141-1136(94)00049-U

    Article  Google Scholar 

  • LaKind JS, Sobus JR, Goodman M, Barr DB, Fürst P, Albertini RJ, Arbuckle TE, Schoeters G, Tan YM, Teeguarden J, Tornero-Velez R, Weiselm CP (2014) A proposal for assessing study quality: Biomonitoring, Environmental Epidemiology, and Short-lived Chemicals (BEES-C) instrument. Environ Int 73:195–207. https://doi.org/10.1016/j.envint.2014.07.01

    Article  CAS  Google Scholar 

  • Lang T, Wosniok W, Baršienė J, Broeg K, Kopecka J, Parkkonen J (2006) Liver histopathology in Baltic flounder (Platichthys flesus) as indicator of biological effects of contaminants. Mar Pollut Bull 53(8-9):488–496. https://doi.org/10.1016/j.marpolbul.2005.11.008

    Article  CAS  Google Scholar 

  • Lavado R, Ureña R, Martin-Skilton R, Torreblanca A, Del Ramo J, Raldúa D, Porte C (2006) The combined use of chemical and biochemical markers to assess water quality along the Ebro River. Environ Pollut 139(2):330–339. https://doi.org/10.1016/j.envpol.2005.05.003

    Article  CAS  Google Scholar 

  • Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev Med Vet 154(6):427–430

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lyons BP, Stentiford GD, Green M, Bignell J, Bateman K, Feist SW, Goodsir F, Reynolds J, Thain JE (2004) DNA adduct analysis and histopathological biomarkers in European flounder (Platichthys flesus) sampled from UK estuaries. Mutat Res Fundam Mol Mech Mutagen 552(1):177–186

    Article  CAS  Google Scholar 

  • Machala M, Dusek L, Hilscherova K, Kubinova R, Jurajda P, Neca J, Ulrich R, Gelnar M, Studnickova Z, Holoubek I (2001) Determination and multivariate statistical analysis of biochemical responses to environmental contaminants in feral freshwater fish Leuciscus cephalus L. Environ Toxicol Chem Int J 20(5):1141–1148. https://doi.org/10.1002/etc.5620200528

    Article  CAS  Google Scholar 

  • Mani R, Meena B, Valivittan K, Suresh A (2014) Glutathione-S-transferase and catalase activity in different tissues of marine Catfish (Arius arius) on exposure to cadmium. Int J Pharm Pharm Sci 6(1):326–332

    Google Scholar 

  • Maria VL, Ahmad I, Oliveira M, Serafim A, Bebianno MJ, Pacheco M, Santos MA (2009) Wild juvenile Dicentrarchus labrax L. liver antioxidant and damage responses at Aveiro Lagoon, Portugal. Ecotoxicol Environ Saf 72(7):1861–1870

    Article  CAS  Google Scholar 

  • Martins C, Alves de Matos AP, Costa MH, Costa PM (2015) Alterations in juvenile flatfish gill epithelia induced by sediment-bound toxicants: a comparative in situ and ex situ study. Mar Environ Res 112:122–130

    Article  CAS  Google Scholar 

  • Martins M, Santos JM, Costa MH, Costa PM (2016) Applying quantitative and semi-quantitative histopathology to address the interaction between sediment-bound polycyclic aromatic hydrocarbons in fish gills. Ecotoxicol Environ Saf 131:164–171. https://doi.org/10.1016/j.ecoenv.2016.04.019

    Article  CAS  Google Scholar 

  • Metcalfe CD, Balch GC, Cairns VW, Fitzsimons JD, Dunn BP (1990) Carcinogenic and genotoxic activity of extracts from contaminated sediments in western Lake Ontario. Sci Total Environ 94(1-2):125–141. https://doi.org/10.1016/0048-9697(90)90368-5

    Article  CAS  Google Scholar 

  • Mikaelian I, de Lafontaine Y, Ménard C, Tellier P, Harshbarger J, Martineau D (1998) Neoplastic and nonneoplastic hepatic changes in lake whitefish (Coregonus clupeaformis) from the St. Lawrence River, Quebec, Canada. Environ Health Perspect 106(4):179–183. https://doi.org/10.1289/ehp.98106179

    Article  CAS  Google Scholar 

  • Monserrat JM, Martínez PE, Geracitano LA, Amado LL, Martins CMG, Pinho GLL, Chaves IS, Cravo MF, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol C Toxicol Pharmacol 146(1-2):221–234. https://doi.org/10.1016/j.cbpc.2006.08.012

    Article  CAS  Google Scholar 

  • Monteiro SM, Rocha E, Fontaínhas-Fernandes A, Sousa M (2008) Quantitative histopathology of Oreochromis niloticus gills after copper exposure. J Fish Biol 73:1376–1392

    Article  CAS  Google Scholar 

  • Morais S, Aragão C, Cabrita E, Conceição LE, Constenla M, Costas B, Dias J, Duncan N, Engrola S, Estevez A, Gisbert E, Mañanós M, Valente LMP, Yúfera M, Dinis (2016) New developments and biological insights into the farming of Solea senegalensis reinforcing its aquaculture potential. Rev Aquac 8(3):227–263. https://doi.org/10.1111/raq.12091

    Article  Google Scholar 

  • Moreira SM, Guilhermino L (2005) The use of Mytilus galloprovincialis acetylcholinesterase and glutathione S-transferases activities as biomarkers of environmental contamination along the northwest Portuguese coast. Environ Monit Assess 105(1-3):309–325. https://doi.org/10.1007/s10661-005-3854-z

    Article  CAS  Google Scholar 

  • Mrozik A, Piotrowska-Seget Z, Labuzek S (2003) Bacterial degradation and bioremediation of polycyclic aromatic hydrocarbons. Pol J Environ Stud 12(1):15–25

    CAS  Google Scholar 

  • 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, Portugal

  • Myers MS, Johnson LL, Hom T, Collier TK, Stein JE, Varanasi U (1998) Toxicopathic hepatic lesions in subadult English sole (pleuronectes vetuls) from Puget Sound, Washington, USA: relationships with other biomarkers of contaminant exposure. Mar Environ Res 45(1):47–67. https://doi.org/10.1016/S0141-1136(97)00021-4

    Article  CAS  Google Scholar 

  • Nero V, Farwell A, Lee LEJ, Van Meer T, MacKinnon MD, Dixon DG (2006) The effects of salinity on naphthenic acid toxicity to yellow perch: gill and liver histopathology. Ecotoxicol Environ Saf 65(2):252–264. https://doi.org/10.1016/j.ecoenv.2005.07.009

    Article  CAS  Google Scholar 

  • Nunes B, Brandão F, Sérgio T, Rodrigues S, Correia AT (2014) Effects of environmentally relevant concentrations of metallic compounds on the flatfish Scophtalmus maximus: biomarkers of neurotoxicity, oxidative stress, and metabolism. Environ Sci Pollut Res 21:7501–7511. https://doi.org/10.1007/s11356-014-2630-4

    Article  CAS  Google Scholar 

  • Nunes B, Verde MF, Soares AM (2015) Biochemical effects of the pharmaceutical drug paracetamol on Anguilla anguilla. Environ Sci Pollut Res Int 22(15):11574–11584. https://doi.org/10.1007/s11356-015-4329-6. Epub 2015

  • OECD (2000) Test No. 215: Fish, Juvenile Growth Test. OECD Guidelines for the testing of Chemicals

  • Oliva M, Garrido C, Sales D, de Canales MLG (2008) Lindane toxicity on early life stages of gilthead seabream (Sparus aurata) with a note on its histopathological manifestations. Environ Toxicol Pharmacol 25(1):94–102. https://doi.org/10.1016/j.etap.2007.09.005

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Oliveira M, Pacheco M, Santos MA (2008) Organ specific antioxidant responses in golden grey mullet (Liza aurata) following a short-term exposure to phenanthrene. Sci Total Environ 396(1):70–78. https://doi.org/10.1016/j.scitotenv.2008.02.012

    Article  CAS  Google Scholar 

  • Oliveira M, Maria VL, Ahmad I, Serafi A, Bebianno MJ, Pacheco M, Santos MA (2009) Contamination assessment of a coastal lagoon (Ria de Aveiro, Portugal) using defense and damage biochemical indicators in gill of Liza aurata-an integrated biomarker approach. Environ Pollut 157(3):959–967. https://doi.org/10.1016/j.envpol.2008.10.019

    Article  CAS  Google Scholar 

  • Olsson P-E, Larsson Å, Haux C (1996) Influence of seasonal changes in water temperature on cadmium inducibility of hepatic and renal metallothionein in rainbow trout. Mar Environ Res 42(1-4):41–44. https://doi.org/10.1016/0141-1136(95)00072-0

    Article  CAS  Google Scholar 

  • Pathiratne A, Hemachandra CK (2010) Modulation of ethoxyresorufin O-deethylase and glutathione S-transferase activities in Nile tilapia (Oreochromis niloticus) by polycyclic aromatic hydrocarbons containing two to four rings: implications in biomonitoring aquatic pollution. Ecotoxicology 19(6):1012–1018. https://doi.org/10.1007/s10646-010-0482-3

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Reis PA, Antunes JC, Almeida CMR (2009) Metal levels in sediments from the Minho estuary salt marsh: a metal clean area? Environ Monit Assess 159(1–4):191–205. https://doi.org/10.1007/s10661-008-0622-x

    Article  CAS  Google Scholar 

  • Ribeiro OCA, Vollaire Y, Sanchez-Chardi A, Roche H (2005) Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquat Toxicol 74(1):53–69. https://doi.org/10.1016/j.aquatox.2005.04.008

    Article  CAS  Google Scholar 

  • Richmonds C, Dutta HM (1989) Histopathological changes induced by malathion in the gills of blue gill Lepomis macrochirus. Bull Environ Contam Toxicol 43(1):123–130. https://doi.org/10.1007/BF01702248

    Article  CAS  Google Scholar 

  • Rodrigues S, Antunes SC, Nunes B, Correia AT (2017) Histological alterations in gills and liver of rainbow trout (Oncorhynchus mykiss) after exposure to the antibiotic oxytetracycline. Environ Toxicol Pharmacol 53:164–176. https://doi.org/10.1016/j.etap.2017.05.012

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sarasquete C, González de Canales ML, Arellano JM, Munõz-Cueto JA, Ribeiro L, Dinis MT (1998) Histochemical study of skin and gills of Senegal sole, Solea senegalensis larvae and adults. Histol Histopathol 13:727–735

    CAS  Google Scholar 

  • Sayed AEDH, Mekkawy IA, Mahmoud UM (2012) Histopathological alterations in some body organs of adult Clarias Gariepinus (Burchell, 1822) exposed to 4-nonylphenol, Zoology. In: Garcia MD (ed) InTech, West Palm Beach, pp 163–184

  • Schwaiger 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(1):75–86. https://doi.org/10.1023/A:1008212000208

    Article  CAS  Google Scholar 

  • 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 Forurensnings Tilsyn (SFT), Norwegian Pollution Control Authority SFT TA-2229/2007

  • Shabana MB, Ibrahim HM, Khadre SEM, Elemam MG (2012) Influence of rifampicin and tetracycline administration on some biochemical and histological parameters in albino rats. J Basic Appl Zool 65(5):299–308. https://doi.org/10.1016/j.jobaz.2012.10.009

    Article  CAS  Google Scholar 

  • Simpson MG (1992) Histopathological changes in the liver of dab (Limanda limanda) from a contamination gradient in the North Sea. Mar Environ Res 34(1-4):39–43. https://doi.org/10.1016/0141-1136(92)90080-6

    Article  Google Scholar 

  • Simpson MG, Parry M, Kleinkauf A, Swarbreck D, Walker P, Leah RT (2000) Pathology of the liver, kidney and gonad of flounder (Platichthys flesus) from a UK estuary impacted by endocrine disrupting chemicals. Mar Environ Res 50(1-5):283–287. https://doi.org/10.1016/S0141-1136(00)00089-1

    Article  CAS  Google Scholar 

  • Soegianto A, Charmantier-Daures M, Trilles JP, Charmantier G (1999) Impact of copper on the structure of gills and epipodites of the shrimp Penaeus japonicus (Decapoda). J Crustac Biol 19(2):209–223. https://doi.org/10.1163/193724099X00015

    Article  Google Scholar 

  • Solangi MA, Overstreet RM (1982) 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(1):13–35. https://doi.org/10.1111/j.1365-2761.1982.tb00453.x

    Article  CAS  Google Scholar 

  • Solé M, Vega S, Varó I (2012) Characterization of type “B” esterases and hepatic CYP450 isoenzimes in Senegalese sole for their further application in monitoring studies. Ecotoxicol Environ Saf 78:72–79. https://doi.org/10.1016/j.ecoenv.2011.11.013

    Article  CAS  Google Scholar 

  • Solé M, Fortuny A, Mañanós E (2014) Effects of selected xenobiotics on hepatic and plasmatic biomarkers in juveniles of Solea senegalensis. Environ Res 135:227–235. https://doi.org/10.1016/j.envres.2014.09.024

  • Soltani N, Amira A, Sifi K, Beldi H (2012) Environmental monitoring of the Annaba gulf (Algeria): measurement of biomarkers in Donax trunculus and metallic pollution. Bull Soc Zool Fr 137(1-4):51–60

    Google Scholar 

  • Stohs SJ, Bagchi D, Hassoun E, Bagchi M (2000) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 20(2):12. https://doi.org/10.1615/JEnvironPatholToxicolOncol.v20.i2.10

    Article  Google Scholar 

  • Storey KB (1996) Oxidative stress: animal adaptations in nature. Braz J Med Biol Res 29:1715–1733

    CAS  Google Scholar 

  • Tabet F, Touyz RM (2007) Reactive oxygen species, oxidative stress, and vascular biology in hypertension. Comprehensive hypertension, edition, pp 337–44

  • 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

    Article  CAS  Google Scholar 

  • Viarengo A, Canesi L, Pertica M, Livingstone DR (1991) Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels. Comp Biochem Physiol C 100(1-2):187–190. https://doi.org/10.1016/0742-8413(91)90151-I

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wilson JM, Bunte RM, Carty AJ (2009) Evaluation of rapid cooling and tricaine methanesulfonate (MS222) as methods of euthanasia in zebrafish (Danio rerio). J Am Assoc Lab Anim Sci 48(6):785–789

    CAS  Google Scholar 

  • Wolf JC, Baumgartner WA, Blazer VS, Camus AC, Engelhardt JA, Fournie JW, Salvatore Frasca Jr S, Groman DB, Kent ML, Khoo LH, Law JM, Lombardini ED, Ruehl-Fehlert C, Segner HE, Smith SA, Spitsbergen JM, Weber K, Wolfe MJ (2015) Nonlesions, misdiagnoses, missed diagnoses, and other interpretive challenges in fish histopathology studies: a guide for investigators, authors, reviewers, and readers. Toxicol Pathol 43:297–325

    Article  Google Scholar 

  • Yasser AG, Naser MD (2011) Impact of pollutants on fish collected from different parts of Shatt Al-Arab River: a histopathological study. Environ Monit Assess 181(1-4):175–182. https://doi.org/10.1007/s10661-010-1822-8

    Article  Google Scholar 

  • Zaghden H, Kallel M, Louati A, Elleuch B, Oudot J, Saliot A (2005) Hydrocarbons in surface sediments from the Sfax coastal zone, (Tunisia). Mediterranean Sea. Mar Pollut Bull 50(11):1287–1294. https://doi.org/10.1016/j.marpolbul.2005.04.045

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zhao Y-Q, Liu G-D, Hou CC, Han YL, Zhu JQ (2016) Effect of cadmium exposure on antioxidant enzyme catalase in different tissues of Acrossocheilus fasciatus. Mol Cell Toxicol 12(3):255–263. https://doi.org/10.1007/s13273-016-0030-1

    Article  CAS  Google Scholar 

  • Zhou JL, Fileman TW, Evans S, Donkin P, Readman JW, Mantoura RFC, Rowland S (1999) The partition of fluoranthene and pyrene between suspended particles and dissolved phase in the Humber Estuary: a study of the controlling factors. Sci Total Environ 243:305–321. https://doi.org/10.1016/S0048-9697(99)00404-0

    Article  Google Scholar 

Download references

Acknowledgments

We 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 Tunisian Ministry of Higher Education and Scientific Research also supported this research study. This work was conducted in the framework of Researcher FCT Program (Operational Program for Human Potential, QREN, EU) which hired Bruno Nunes (IF/01744/2013). We are particularly thankful to Prof. Abdelmajid Dammak for his contribution to correct grammatical errors and to improve the English writing skills of this paper.

Funding

This research was financially 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/04423/2019.

Author information

Authors and Affiliations

  1. Laboratoire d’Ingénierie de l’Environnement et d’Ecotechnologie, ENIS, Université de Sfax, BP 1173, 3038, Sfax, Tunisia

    Rayda Ghribi & Boubaker Elleuch

  2. Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos S/N, 4450-208, Porto, Matosinhos, Portugal

    Rayda Ghribi & Alberto Teodorico Correia

  3. Centro de Estudos do Ambiente e do Mar (CESAM), Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    Rayda Ghribi & Bruno Nunes

  4. Faculdade de Ciências da Saúde da Universidade Fernando Pessoa (FCS/UFP), Rua Carlos da Maia 296, 4200-150, Porto, Portugal

    Alberto Teodorico Correia

  5. Departamento de Biologia, Universidade de Aveiro, Campus de Santiago, 3810-193, Aveiro, Portugal

    Bruno Nunes

Authors
  1. Rayda Ghribi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alberto Teodorico Correia
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Boubaker Elleuch
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bruno Nunes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Bruno Nunes.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Responsible editor: Cinta Porte

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghribi, R., Correia, A.T., Elleuch, B. et al. Testing the impact of contaminated sediments from the southeast marine coast of Tunisia on biota: a multibiomarker approach using the flatfish Solea senegalensis. Environ Sci Pollut Res 26, 29704–29721 (2019). https://doi.org/10.1007/s11356-019-05872-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05872-x

Keywords

Search

Navigation