Skip to main content
SpringerLink
Log in

Immune biomarker and hydrocarbon concentrations in carpet shell clams (Ruditapes decussatus) collected from a Mediterranean coastal lagoon

  • Original Paper
  • Published:
Euro-Mediterranean Journal for Environmental Integration Aims and scope Submit manuscript

Abstract

Immunological alterations may be used as ecotoxicological biomarkers to detect and monitor biological effects of chemical contaminants in polluted environments. The main goal of this study was to assess the immunotoxic effects of hydrocarbon contamination in the soft tissues of carpet shell clams (Ruditapes decussatus) sampled from the South Lagoon of Tunis (Tunisia). Sediments and clams were collected from four locations, three of which were located within the polluted South Lagoon of Tunis (S1, S2 and S3) whereas the other was a clean site on the Mediterranean coast. Total hydrocarbons were extracted from the clam tissues and sediments and fractionated into aromatic and nonaromatic hydrocarbons. The status of the clam immune system was assessed by measuring the total haemocyte count (THC) and the phenoloxidase, lysozyme and esterase activities in haemolymph samples from the clams. Hydrocarbon analysis revealed that pollution levels in the South Lagoon of Tunis were high and spatially variable. Phenoloxidase activity was inhibited in clams sampled at sites S1, S2 and S3 compared to clams at the control site, while lysozyme and esterase activities and THCs were higher in the clams at the polluted sites than in those at the control site. Moreover, the biomarker responses indicated that S3 was the most polluted site in the South Lagoon of Tunis. The results of the present study clearly show that suitable biomarkers can be useful tools for biomonitoring in the study area.

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

  • Abdel-Shafy HI, Mansour MS (2016) A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt J Pet 25:107–123

    Article  Google Scholar 

  • Abrajano T Jr, Yan B, O'Malley V (2003) High molecular weight petrogenic and pyrogenic hydrocarbons in aquatic environments. Treatise Geochem 9:612

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Asokan R, Arumugam M, Mullainadhan P (1997) Activation of prophenoloxidase in the plasma and haemocytes of the marine mussel Perna viridis Linnaeus. Dev Comp Immunol 21:1–12

    Article  Google Scholar 

  • Bado-Nilles A, Gagnaire B, Thomas-Guyon H, Le Floch S, Renault T (2008) Effects of 16 pure hydrocarbons and two oils on haemocyte and haemolymphatic parameters in the Pacific oyster, Crassostrea gigas (Thunberg). Toxicol Vitro 22:1610–1617

    Article  Google Scholar 

  • Bado-Nilles A, Quentel C, Auffret M, Le Floch S, Gagnaire B, Renault T, Thomas-Guyon H (2009) Immune effects of HFO on European sea bass, Dicentrarchus labrax, and Pacific oyster, Crassostrea gigas. Ecotoxicol Environ Saf 72:1446–1454

    Article  Google Scholar 

  • Bado-Nilles A, Renault T, Faury N, Le Floch S, Quentel C, Auffret M, Thomas-Guyon H (2010) In vivo effects of LCO soluble fraction on immune-related functions and gene transcription in the Pacific oyster, Crassostrea gigas (Thunberg). Aquat Toxicol 97:196–203

  • 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

    Article  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Anal Biochem 72:248–255

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 Impacts 18:895–907

    Article  Google Scholar 

  • 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 6:28–33

  • Chalghmi H, Bourdineaud J-P, Chbani I, Haouas Z, Bouzid S, Er-Raioui H, Saidane-Mosbahi D (2020) Occurrence, sources and effects of polycyclic aromatic hydrocarbons in the Tunis lagoon, Tunisia: an integrated approach using multi-level biological responses in Ruditapes decussatus. Environ Sci Pollut Res 27:3661–3674

  • Cheng TC, Rodrick GE, Foley DA, Koehler SA (1975) Release of lysozyme from hemolymph cells of Mercenaria mercenaria during phagocytosis. J Invertebr Pathol 25:261–265

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cotou E, Tsangaris C, Henry M (2013) Comparative study of biochemical and immunological biomarkers in three marine bivalves exposed at a polluted site. Environ Sci Pollut Res 20:1812–1822

    Article  Google Scholar 

  • Croxton AN, Wikfors GH, Schulterbrandt-Gragg RD (2012) Immunomodulation in eastern oysters, Crassostrea virginica, exposed to a PAH-contaminated, microphytobenthic diatom. Aquat Toxicol 118–119:27–36. https://doi.org/10.1016/j.aquatox.2012.02.023

    Article  Google Scholar 

  • Díaz-Resendiz K, Romero-Bañuelos C, Robledo-Marenco M, Rojas-García A, Barrón-Vibanco B, Medina-Díaz I, Girón-Pérez M (2014) Deregulation of the humoral immune response of the oyster (Crassostrea corteziensis) exposed to naphthalene. Invert Surviv J 11:30–38

    Google Scholar 

  • Duchemin MB, Auffret M, Wessel N, Fortier M, Morin Y, Pellerin J, Fournier M (2008) Multiple experimental approaches of immunotoxic effects of mercury chloride in the blue mussel Mytilus edulis, through in vivo, in tubo and in vitro exposures. Environ Pollut 153:416–423

  • Dyrynda EA, Law RJ, Dyrynda PE, Kelly CA, Pipe RK, Ratcliffe NA (2000) Changes in immune parameters of natural mussel Mytilus edulis populations following a major oil spill (Sea Empress, Wales, UK). Mar Ecol Prog Ser 206:155–170

  • Er-Raioui H, Bouzid S, Marhraoui M, Saliot A (2009) Hydrocarbon pollution of the Mediterranean coastline of Morocco. Ocean Coast Manag 52:124–129

    Article  Google Scholar 

  • Esposito G et al (2018) The bivalve Ruditapes decussatus: a biomonitor of trace elements pollution in Sardinian coastal lagoons (Italy). Environ Pollut 242:1720–1728

  • Fathallah S, Medhioub MN, Kraiem MM (2013) Sediment contact assay using the carpet shell clam, Ruditapes decussatus L., embryos and larvae for assessing contamination levels of four sites in Tunisian coast. Bull Environ Contam Toxicol 90:611–615

    Article  Google Scholar 

  • Gagnaire B, Frouin H, Moreau K, Thomas-Guyon H, Renault T (2006) Effects of temperature and salinity on haemocyte activities of the Pacific oyster, Crassostrea gigas (Thunberg). Fish Shellfish Immunol 20:536–547. https://doi.org/10.1016/j.fsi.2005.07.003

  • Guardiola FA, Cuesta A, Arizcun M, Meseguer J, Esteban MA (2014) Comparative skin mucus and serum humoral defence mechanisms in the teleost gilthead seabream (Sparus aurata). Fish. Shellfish. Immunol. 36:545–551

    Article  Google Scholar 

  • Haberkorn H et al (2014) Cellular and biochemical responses of the oyster Crassostrea gigas to controlled exposures to metals and Alexandrium minutum. Aquat Toxicol 147:158–167. https://doi.org/10.1016/j.aquatox.2013.12.012

  • Hannam ML, Bamber SD, Moody JA, Galloway TS, Jones MB (2009) Immune function in the Arctic Scallop, Chlamys islandica, following dispersed oil exposure. Aquat Toxicol 92:187–194. https://doi.org/10.1016/j.aquatox.2009.01.010

    Article  Google Scholar 

  • Hannam ML, Bamber SD, Galloway TS, John Moody A, Jones MB (2010a) Effects of the model PAH phenanthrene on immune function and oxidative stress in the haemolymph of the temperate scallop Pecten maximus. Chemosphere 78:779–784. https://doi.org/10.1016/j.chemosphere.2009.12.049

    Article  Google Scholar 

  • Hannam ML, Bamber SD, Moody AJ, Galloway TS, Jones MB (2010b) Immunotoxicity and oxidative stress in the Arctic scallop Chlamys islandica: effects of acute oil exposure. Ecotoxicol Environ Saf 73:1440–1448. https://doi.org/10.1016/j.ecoenv.2010.06.012

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hurtado MÁ, Da Silva PM, Le Goïc N, Palacios E, Soudant P (2011) Effect of acclimatization on hemocyte functional characteristics of the Pacific oyster (Crassostrea gigas) and carpet shell clam (Ruditapes decussatus). Fish Shellfish Immunol 31:978–984

  • Jouini Z, Charrada RB, Moussa M (2005) Caractéristiques du Lac Sud de Tunis après sa restauration Mar. Life 15:3–11

    Google Scholar 

  • Khedir-Ghenim Z, Zrafi-Nouira I, Bahri R, Belayouni H, Hammami M, Rouabhia M, Saidane-Mosbahi D (2009) Identification and distribution of petroleum hydrocarbons in sediments, seawater and Ruditapes decussatus collected from a Mediterranean Sea site. Int J Water 5:35–50

    Article  Google Scholar 

  • Luna-Acosta A, Bustamante P, Godefroy J, Fruitier-Arnaudin I, Thomas-Guyon H (2010) Seasonal variation of pollution biomarkers to assess the impact on the health status of juvenile Pacific oysters Crassostrea gigas exposed in situ. Environ Sci Pollut Res 17:999–1008

    Article  Google Scholar 

  • Manoli E, Samara C (2008) The removal of polycyclic aromatic hydrocarbons in the wastewater treatment process: experimental calculations and model predictions. Environ Pollut 151:477–485. https://doi.org/10.1016/j.envpol.2007.04.009

  • Mansour C, Guardiola FA, Esteban MÁ, Mosbahi DS (2017) Combination of polycyclic aromatic hydrocarbons and temperature exposure: In vitro effects on immune response of European clam (Ruditapes decussatus). Fish Shellfish Immunol 67:110–118

    Article  Google Scholar 

  • 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 Ind 19:191–205

    Article  Google Scholar 

  • Matozzo V, Giacomazzo M, Finos L, Marin MG, Bargelloni L, Milan M (2013) Can ecological history influence immunomarker responses and antioxidant enzyme activities in bivalves that have been experimentally exposed to contaminants? A new subject for discussion in “eco-immunology” studies. Fish Shellfish Immunol 35:126–135

    Article  Google Scholar 

  • 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 (south-western Mediterranean Sea). Environ Tec 32:43–54

    Article  Google Scholar 

  • 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. https://doi.org/10.1016/S0025-326X(99)00094-6

    Article  Google Scholar 

  • Parry RM Jr, Chandan RC, Shahani KM (1965) A rapide and sensitive assay of muramidase. Proc Soc Exp Biol Med 119:384–386

    Article  Google Scholar 

  • Pretti C, Cognetti-Varriale AM (2001) The use of biomarkers in aquatic biomonitoring: the example of esterases. Aquat Conserv 11:299–303

    Article  Google Scholar 

  • Reynaud S, Deschaux P (2006) The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review. Aquat Toxicol 77:229–238

    Article  Google Scholar 

  • Romeo 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

    Article  Google Scholar 

  • Solé M (2000) Assessment of the results of chemical analyses combined with the biological effects of organic pollution on mussels. TrAC Trends Anal Chem 19:1–9

  • Turja R, Soirinsuo A, Budzinski H, Devier MH, Lehtonen KK (2013) Biomarker responses and accumulation of hazardous substances in mussels (Mytilus trossulus) transplanted along a pollution gradient close to an oil terminal in the Gulf of Finland (Baltic Sea). Comp Biochem Physiol C 157:80–92. https://doi.org/10.1016/j.cbpc.2012.09.006

  • 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. https://doi.org/10.1016/j.marenvres.2016.11.010

    Article  Google Scholar 

  • Walker CH, Hopkin SP, Sibly RM, Peakall DB (2001) Principles of Ecotoxicology, 2nd edn. Taylor & Francis, London

    Google Scholar 

  • Wootton E, Dyrynda E, Pipe R, Ratcliffe N (2003) Comparisons of PAH-induced immunomodulation in three bivalve molluscs. Aquat Toxicol 65:13–25

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

Acknowledgements

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

Author information

Authors and Affiliations

  1. Laboratory of Analysis, Treatment and Valorization of Pollutants of the Environment and Products, Faculty of Pharmacy, University of Monastir, Ibn Sina Street, 5000, Monastir, Tunisia

    Chalbia Mansour, Fadia Ben Taheur, Rahma Omrani & Dalila Saidane Mosbahi

Authors
  1. Chalbia Mansour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fadia Ben Taheur
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rahma Omrani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dalila Saidane Mosbahi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chalbia Mansour.

Ethics declarations

Conflict of interest

On behalf of all the authors, the corresponding author states that there is no conflict of interest.

Additional information

Communicated by Settimio Ferlisi, Chief Editor.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mansour, C., Taheur, F.B., Omrani, R. et al. Immune biomarker and hydrocarbon concentrations in carpet shell clams (Ruditapes decussatus) collected from a Mediterranean coastal lagoon. Euro-Mediterr J Environ Integr 5, 11 (2020). https://doi.org/10.1007/s41207-020-0147-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s41207-020-0147-4

Keywords

Search

Navigation