Abstract
The aim of our study is to evaluate the impact of Bousfer desalination plant brine discharges on the Algerian west coast, on a natural population of the marine gastropod mollusc Patella rustica. The effects of a chronic exposure to such discharges are complex to understand due to the combined effects of environmental physico-chemical parameters (e.g., high salinity) and different pollutants that can modulate the physiological responses of this species to stress. In this context, we assessed the biological effects in a marine species P. rustica, by a multibiomarker approach that provided information on the health status of organisms in response to such an environmental stress. We measured biomarkers in the whole soft tissues of limpets as indicators of neurotoxicity (AChE activity), oxidative stress (CAT, SOD, GR, and GPx activities), biotransformation (GST), oxidative damage (LPO through TBARS levels), and genotoxicity (CSP 3-like activity). In parallel, hydrological parameters were measured in the Bay of Oran, at four selected sites: site H considered as a “hotspot,” located at Bousfer desalination plant; two other sites E and W, at the east and the west of H respectively; finally, site R “reference” located in Madragh, which is considered as a remote clean site. Our analyses revealed that the activities of antioxidant defense enzymes reached the highest levels in P. rustica collected from site H. The activation of antioxidant defense system in these organisms translated the alteration of their status health, reflecting a level of environmental disruption generated by the desalination plant brine discharges and the high salinity in this area. We also observed that the tissues of limpets collected from site H as well as the two other sites, E and W, had undergone molecular damage, confirmed by the high levels of CSP 3-like activity. This damage resulted from chronic exposure to environmental conditions, potentially genotoxic, due to the desalination plant discharges. The present results indicate the adverse impact of brine effluents from desalination plants on marine fauna and suggest the need for a more consistent approach to environmental management of brine discharges.
Similar content being viewed by others
References
Aebi H (1984) Catalase in vitro. Methods Enzymol 105:21–126
Al-Mutaz I (1991) Environmental impact of seawater desalination plants. Environ Monit Assess 16:75–84
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 155:34–42
Ansaldo M, Najle R, Luquet CM (2005) Oxidative stress generated by diesel seawater contamination in the digestive gland of the Antarctic limpet Nacella concinna. Mar Environ Res 59:381–390
Asatiani N, Sapojnikova N, Abuladze M, Kartvelishvili T, Kulik-ova N, Kiziria E, Namchevadze E, Holman HY (2004) Effects of Cr (VI) long-term and low-dose action on mammalian antioxidant enzymes (an in vitro study). Inorg Biochem 98:6–490
Bebianno MJ, Cravo A, Miguel C, Morais S (2003) Metallothionein concentrations in a population of Patella aspera: variation with size. Sci Total Environ 301:151–161
Belatoui A, Bouabessalam H, Rouane Hacene O, De-la-Ossa-Carretero JA, Martinez-Garcia E, Sanchez-Liza JL (2017) Environmental effects of brine discharge from two desalination plants in Algeria (South Western Mediterranean). Desal water treat 76:311–318
Benali I, Boutiba Z, Merabet A, Chèvre N (2015) Integrated use of biomarkers and condition indices in mussels (Mytilus galloprovincialis) for monitoring pollution and development of biomarker index to assess the potential toxic of coastal sites. Marine Poll Bull 95:385–394
Boyé H (2008) Water, energy, desalination and climate change in the Mediterranean. Sophia Antipolis: Plan Bleu, Regional Activity Center, Environment and Development in the Mediterranean, p. 35 (in French). http://planbleu.org/sites/default/files/publications/eau_energie_dessalement_cc_fr.pdf
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Brecken-Folse JA, Mayer FL, Pedigo LE, Marking LL (1994) Acute toxicity of 4-nitrophenol, 2,4-dinitrophenol, terbufos and trichlorfon to grass shrimp (Palaemonetes spp.) and sheepshead minnows (Cyprinodon variegatus) as affected by salinity and temperature. Environ Toxicol Chem 13:67–77
Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Meth Enzymol 52:302–310
Cailleaud K, Maillet G, Budzinski H, Souissi S, Forget-Leray J (2007) Effects of salinity and temperature on the expression of enzymatic biomarkers in Eurytemora affinis (Calanoida, Copep-oda). Comp Biochem Physiol A 147:841–849
Clairbone A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods of oxygen radical research. CRC Press, Boca Raton, pp 283–284
Cravo A, Bebianno MJ, Foster P (2004) Partitioning of trace metals between soft tissues and shells of Patella aspera. Environ Int 30:87–98
Dellali M, Romeo M, Aissa P (2001) Suivi annuel de l’activité catalase chez des moules et des palourdes originaires de la lagune de Bizerte. Oceanol Acta 24:263–271
Douhri H, Sayah F (2009) The use of enzymatic biomarkers in two marine invertebrates Nereis diversicolor and Patella vulgata for the biomonitoring of Tangier’s bay (Morocco). Ecotoxicol Environ Saf 72:394–399
Edison B, Eduardo Tavares P (2011) The use of oxygen consumption and ammonium excretion to evaluate the toxicity of cadmium on Farfantepenaeus paulensis with respect to salinity. Chemosphere 84:9–16
Elimelech M, Phillip WA (2011) The future of seawater desalination: energy, technology, and the environment. Science 333:712–717
Ellman GL, Courtney KD, Andreas V, Featherstone RM (1961) A new and rapid colorimetric determination of AChE activity. Biochem Pharmacol 7:88–95
Feig C, Peter ME (2007) How apoptosis got the immune system in shape. Eur J Immunol 37:61–70
Fernández-Torquemada Y, González-Correa JM, Sánchez-Lizaso JL (2013) Echinoderms as indicators of brine discharge impacts. Desal Water Treat 51:567–557
Forget J, Beliaeff B, Bocquené G (2003) Acetylcholinesterase activity in copepods (Tigriopus brevicornis) from the Vilaine River estuary, France, as a biomarker of neurotoxic contaminants. Aquat Toxicol 62:195–204
Foster P, Chacko J (1995) Minor and trace elements in the shell of Patella vulgata (L.) Mar Environ Res 40:55–76
Freire CA, Togni VG, Hermes-Lima M (2011) Responses of free radical metabolism to air exposure or salinity stress, in crabs (Callinectes danae and C. ornatus) with different estuarine distributions. Comp Biochem Physiol A 160:291–300
Gacia E, Invers O, Manzanera M, Ballesteros E, Romero J (2007) Impact of the brine from a desalination plant on a shallow seagrass (Posidonia oceanica) meadow. Estuar Coast Shelf Sci 72:579–590
Galgani F, Bocquené G (1991) Semi-automated colorimetric and enzymatic assays for aquatic organisms using microplate readers. Water Res 25:147–150
Garrote-Moreno A, Fernández-Torquemada Y, Sánchez-Lizaso JL (2014) Salinity fluctuation of the brine discharge affects growth and survival of the seagrass Cymodocea nodosa. Mar Pollut Bull 81:61–68
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases The first step in mercapturic acid formation. J Biol Chem 249:7120–7130
Halliwell B (2007) Biochemistry of oxidative stress. Biochem Soc Trans 35:1147–1150
Halliwell B, Gutteridge JMC (1985) Free radicals in biology and medecine. Clarendon Press, Oxford, p 331
Henry RP, Gehnrich S, Weihrauch D, Towle DW (2003) Salinity mediated carbonic anhydrase induction in the gills of the euryhaline green crab, Carcinus maenas. Comp Biochem Physiol A 136:243–258
Intanai I, Taylor EW, Whiteley NM (2009) Effects of salinity on rates of protein synthesis and oxygen uptake in the post-larvae and juveniles of the tropical prawn Macrobrachium rosenbergii (de Man). Comp Biochem Physiol A 152:372–378
Jenkins S, Paduan J, Roberts PH, Schlenk D, Weis J (2013) Management of brine discharges to coastal waters recommendations of a science advisory panel, Southern California Coastal Water Research Project. Technical Report, Costa Mesa, CA, p 694
Jimenez Del Rio M, Velez-Pardo C (2004) Transition metal-induced apoptosis in lymphocytes via hydro radical generation, mitochon- dria dysfunction, and caspase-3 activation: an in vitro model for neurodegeneration. Arch Med Res 35:93–185
Khessiba A, Roméo M, Aïssa P (2005) Effects of some environmental parameters on catalase activity measured in the mussel (Mytilus galloprovincialis) exposed to lindane. Environ Pollut 133:275–281
Lattemann S, Höpner T (2008) Environmental impact and impact assessment of seawater desalination. Desalination 220:1–15
Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71:952–958
Liu Y, Wang WN, Wang AL, Wang JM, Sun RY (2007) Effects of dietary vitamin E supplementation on antioxidant enzyme activities in Litopenaeus vannamei (Boone, 1931) exposed to acute salinity changes. Aquaculture 265:351–358
Locatello L, Matozzo V, Marin M (2009) Biomarker responses in the crab Carcinus aestuarii to assess environmental pollution in the Lagoon of Venice (Italy). Ecotoxicology 18:869–877
Mc Cord J, Fridovich I (1969) Superoxide dismutase, an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244:6046–6055
Menezes S, Soares A, Guilhermino L, Peck MR (2006) Biomarker responses of the estuarine brown shrimp Crangon crangon L. to non-toxic stressors: temperature, salinity and handling stress effects. J Exp Mar Biol Ecol 335:114–122
Mičić M, Bihari N, Željko J (2002) DNA damage and apoptosis in the mussel Mytilus galloprovincialis. Mar Environ Res 53:243–262
Millot C (1985) Some features of the Algerian current. J geophy Res 90:7169–7176
Monserrat JM, Martínez PE, Geracitano LA, Amado LL, Martins CM, Pinho GL, 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
Moreira A, Figueira E, Soares AMVM, Freitas R (2016) Salinity influences the biochemical response of Crassostrea angulata to Arsenic. Environ Pollut 214:756–766
Morton AJ, Callister IK, Wade NM (1996) Environmental impacts of seawater distillation and reverse osmosis processes. Dessalination 108:1–10
Mouneyrac C, Buffet PE, Poirier L, Zalouk-Vergnoux A, Guibbolini M, Faverney C, Gilliland D, Berhanu D, Dybowska A, Châtel A, Perrein-Ettajni H, Pan JF, Thomas-Guyon H, Reip P, Valsami-Jones E (2014) Fate and effects of metal-based nanoparticles in two marine invertebrates, the bivalve mollusc Scrobicularia plana and the annelid polychaete Hediste diversicolor. Environ Sci Pollut Res 21:7899–7912
Paital B, Chainy GB (2010) Antioxidant defenses and oxidative stress parameters in tissues of mud crab (Scylla serrata) with reference to changing salinity. Comp Biochem Physiol C: Toxicol Pharmacol 151:142–151
Pfeifer S, Schiedek D, Dippner JW (2005) Effect of temperature and salinity on acetylcholinesterase activity, a common pollution biomarker, in Mytilus sp. from the south-western Baltic Sea. J Exp Mar Biol Ecol 320:93–103
Pham-Huy LA, He H, Pham-Huy C (2008) Free radicals, antioxidants in disease and health. Int J Biomed Sci 4:9–96
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 bio-indicator organisms: a practical model to elaborate data from sediment chemistry, bioavailability, biomarkers and ecotoxicological bioassays. Chemosphere 83:475–485
Reader S, Moutardier V, Denizeau F (1999) Tributyltin triggers apoptosis in trout hepatocytes: the role of Ca2+, protein kinase C and proteases. Biochem Biophys Acta 1448:473–485
Riera R, Tuya F, Sacramento A, Ramos E, Rodríguez M (2011) The effects of brine disposal on a subtidal meiofauna community. Estuar Coast Shelf Sci 93:359–365
Risso-de Faverney C, Devaux A, Lafaurie M, Girard JP, Bailly B, Rahmani R (2001) Cadmium induces apoptosis and genotoxicity in rainbow trout hepatocytes through generation of reactive oxygene species. Aquat Toxicol 53:65–76
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
Rivera-Ingraham GA, Nommick A, Blondeau-Bidet E, Ladurner P, Jehan-Hervé L (2016) Salinity stress from the perspective of the energy-redox axis: lessons from a marine intertidal flatworm. Redox Biol 10:53–64
Rodrigues AP, Correia Oliveira P, Guilhermino L, Guimaraes L (2012) Effects of salinity stress on neurotransmission, energy metabolism, and anti-oxidant biomarkers of Carcinus maenas from two estuaries of the NW Iberian Peninsula. Mar Biol 159:2061–2074
Scaps P, Borot O (2000) Acetylcholinesterase activity of the polychaete Nereis diversicolor: effects of temperature and salinity. Comp Biochem Physiol C, Toxicol Pharmacol 125:377–383
Schiffler M (2004) Perspectives and challenges for desalination in the 21st century. Desalination 165:1-9
Sureda A, Box A, Tejada S, Blanco A, Caixach J, Deudero S (2011) Biochemical responses of Mytilus galloprovincialis as biomarkers of acute environmental pollution caused by the Don Pedro oil spill (Eivissa Island, Spain). Aquat Toxicol 101:540–549
Tu HT, Silvestre F, De Meulder B, Thome JP, Phuong NT, Kestemont P (2012) Combined effects of deltamethrin, temperature and salinity on oxidative stress biomarkers and acetylcholinesterase activity in the black tiger shrimp (Penaeus monodon). Chemosphere 86:83–91
Vargas-Chacoff L, Arjona FJ, Polakof S, del Río MP, Soengas JL, Mancera JM (2009) Interactive effects of environmental salinity and temperature on metabolic responses of gilthead sea bream Sparus aurata. Comp Biochem Physiol A Mol Integr Physiol 154:417–424
Velez C, Figueira E, Soares AMVM, Freitas R (2016) Native and introduced clams biochemical responses to salinity and pH changes. Sci Total Environ 566–567:260–268
Wang J, Zhu X, Huang X, Gu L, Chen Y, Yang Z (2016) Combined effects of cadmium and salinity on juvenile Takifugu obscurus: cadmium moderates salinity tolerance; salinity decreases the toxicity of cadmium. Sci Rep 6:30968
Acknowledgments
This research work is part of a collaborative project, PHC-Maghreb (15MAG23), supported and funded by Campus France. This article is dedicated to Professor Zitouni Boutiba, who left us in November 2016.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Cinta Porte
Rights and permissions
About this article
Cite this article
Benaissa, M., Rouane-Hacene, O., Boutiba, Z. et al. Ecotoxicological impact assessment of the brine discharges from a desalination plant in the marine waters of the Algerian west coast, using a multibiomarker approach in a limpet, Patella rustica . Environ Sci Pollut Res 24, 24521–24532 (2017). https://doi.org/10.1007/s11356-017-0081-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-0081-4