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The use of brown mussel as bioindicator of pesticides pollution in Agadir Bay (Southern Morocco)

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Abstract

The rapid expansion of agriculture in the Souss Massa region has been accompanied by a significant increase in pesticide usage to protect and increase crop yields. Unfortunately, these pesticides leave behind residues that can have detrimental effects on both human health and the environment. To investigate the impact of pesticide contamination on the coasts of Agadir Bay, our study focuses on the bivalve Perna perna (Linnaeus, 1758) as a biomonitoring sentinel species. Between autumn 2009 and summer 2010, we conducted measurements of pesticide residue concentrations and assessed two biomarkers of pollution the Glutathion-S-transferase (GST) and acetylcholinesterase (AChE) in the soft tissues of P. perna. These bivalves were seasonally collected from two different locations along the Agadir Bay coast. The results revealed that Glutathion-S-transferase and acetylcholinesterase showed seasonal variations, likely influenced by the species' reproductive cycle. In terms of pesticide concentrations, the levels of organochlorines were found to range from 13.40 to 109.76 ng g−1 of dry weight (dw) for Dichlofluanide, not-detected (ND) to 38.66 ng g−1 dw for Endosulfan S, ND to 15.76 ng g−1 dw for Lindane, ND to 33.66 ng g−1 dw for Fenarimol, and 0.26–35.02 ng g−1 dw for Buperimate. It should be noted that these levels of pesticide contamination are relatively low compared to values reported in similar studies conducted in other regions of the world. The contamination of Agadir Bay by pesticides can be attributed to their extensive use in agricultural practices in the Souss Massa region.

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The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

References

  • Agnaou M, Ait Alla A, Ouassas M, Bazzi L, El Alami Z, Moukrim A (2014) Assessment of organochlorine pesticides contamination of oued souss estuary (South of Morocco): seasonal variability in sediment and a detritivore annelid Neries diversicolor. J Mater Environ Sci 5:581–586

    CAS  Google Scholar 

  • Agnaou M, Nadir M, Ait Alla A, Bazzi L, El Alami Z, Moukrim A (2018) The occurrence and spatial distribution of pesticides in sea water of the Agadir bay (South of Morocco). J Mater Environ Sci 9(10):3001–3008

    CAS  Google Scholar 

  • Ait Alla A, Mouneyrac C, Durou C, Moukrim A, Pellerin J (2006) Tolerance and biomarkers as useful tools for assessing environmental quality in the Oued Souss estuary (Bay of Agadir, Morocco). Comp Biochem Physiol Part C 143:23–29. https://doi.org/10.1016/j.cbpc.2005.11.015

    Article  CAS  Google Scholar 

  • Alami M (1991) Toxicité des pesticides organochlorés chez les organismes aquatiques : aspects environnementaux et expérimentaux. Thése de 3ème cycle,fac. sci.Rabat. In : Benbakhta B, Fekhaoui M, El Abidi Ab, Idrissi L, Lecorre P (2007) Résidus de pesticides organochlorés chez les bivalves et les poissons de la lagune de Moulay Bousselham (Maroc). https://doi.org/10.4314/afsci.v3i1.61245

  • Aliko V, Multisanti CR, Turani B, Faggio C (2022) Get rid of marine pollution: bioremediation an innovative, attractive, and successful cleaning strategy. Sustainability 14(18):11784

    Article  CAS  Google Scholar 

  • Amiard-Triquet C, Altmann S, Amiard JC, Ballan-Dufrancais C, Baumard P, Budzinski H, Crouzet C, Guarrigues JP, His E, Jeantet AY, Menarsia R, Mora P, Mouneyrac C, Narbonne JF, Pavillon JF (1998) Fate and effects of micropolluants in the Girond estuary, France: a multidisciplinary approach. Hydrobiologia 373(374):259–279. https://doi.org/10.1023/A:1017055118218

    Article  Google Scholar 

  • Amri S, Faouzi M, Fériel S, Ouali K (2017) Seasonal antioxidant responses in the sea urchin Paracentrotus lividus (Lamarck 1816) used as a bioindicator of the environmental contamination in the South-East Mediterranean. Mar Pollut Bull 122(1–2):392–402. https://doi.org/10.1016/j.marpolbul.2017.06.079

    Article  CAS  PubMed  Google Scholar 

  • Azdi M, Moukrim A, Burgeot T, Budzinski H, Chiffoleau JJ, Kaaya A, Zekhnini A, Narbonne JF, Guarrigues P (2006) Hydrocarbon pollution along Moroccan Coasts and BPH activity in the mussel Perna perna. Polycyc Aromat Compd 26:265–282. https://doi.org/10.1080/10406630600904059

    Article  CAS  Google Scholar 

  • Banaoui A, El Hamidi F, Kaaya A, Bouhaimi A, Zekhnini A, Moukrim A (2015) Assessment of multimarker responses in Perna perna, Mytilus galloprovincialis and Donax trunculus bivalves exposed to malathion and 2,4-dichlorophenoxyacetic acid pesticides. J Mater Environ Sci 6(6):1678–1683

    CAS  Google Scholar 

  • Banni M, Ben Dhiab R, El Abed A, Boussetta H (2003) Genetoxicity, catalase and acetylcholinesterase in the assessment of the pollution status of some sites on the Tunisian Littoral. Bull Environ Contam Toxicol 70:854–860. https://doi.org/10.1007/s00128-003-0061-x

    Article  CAS  Google Scholar 

  • Bazzi L, Zougagh M, Salghi R, Hormatallah A, Lemerhyeratte A, Mihit M, Chakir A (2009) Pesticide residue monitoring in green beans from Souss-massa (Morocco) and half-life times of dithiocarbamate fungicide on green beans after field treatments by Mancozeb and Mefenoxam. Orient J Chem 25(3):461–470

    CAS  Google Scholar 

  • Bergayou H, Mouneyrac C, Pellerin J, Moukrim A (2009) Oxidative stress responses in bivalves (Scrobicularia plana, Cerastoderma edule) from the Oued Souss estuary (Morocco). Ecotoxicol Environ Saf 72:765–769. https://doi.org/10.1016/j.ecoenv.2008.09.012

    Article  CAS  PubMed  Google Scholar 

  • Bitar G (1987) Etude de peuplements benthiques littoraux des côtes Atlantiques et Méditerranéennes du Maroc: Impact de la pollution—Comparaison biogéographique. Thèse de Doctorat d'Etat, Université Aix-Marseille II. https://www.theses.fr/1987AIX22005

  • Bligh EG, Dyer WJ (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37:911–917. https://doi.org/10.1139/o59-099

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1016/j.chemosphere.2006.03.049

    Article  ADS  CAS  PubMed  Google Scholar 

  • Bocquené G, Galgani F (1991) Acetylcholinesterase activity in the common prawn (Palaemon serratus) contaminated by carbaryl and Phosalone. Ecotox Environ Saf 22:337–345. https://doi.org/10.1016/0147-6513(91)90083-2

    Article  Google Scholar 

  • Borrell A, Bloch D, Desportes G (1995) Age trends and reproductive transfer of organochlorine compounds in long-finned pilot whales from the Faroe Islands. Environ Pollut 88:283–292. https://doi.org/10.1016/0269-7491(95)93441-2

    Article  CAS  PubMed  Google Scholar 

  • Bouhaimi A (2002) Etude de la biologie des moules Mytilus galloprovincialis et Perna perna et validation de certains biomarqueurs (Ac´etylcholinet´erase et peroxydation lipidique) pour l’´evaluation de l’´etat de sant´e de la baie d’Agadir (Thˇcse d’Etat). Universit´e Ibn Zohr, Facult´e des Sciences, Agadir, p 187

  • Bouzahouane H, Barour Ch, Sleimi N, Ouali K (2018) Multi-biomarkers approach to the assessment of the southeastern Mediterranean Sea health status: Preliminary study on Stramonita haemastoma used as a bioindicator for metal contamination. Chemosphere 207:725–741. https://doi.org/10.1016/j.chemosphere.2018.05.118

    Article  ADS  CAS  PubMed  Google Scholar 

  • 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(2–3):295–311. https://doi.org/10.1016/S0048-9697(99)00499-4

    Article  ADS  CAS  PubMed  Google Scholar 

  • Chahouri A, Agnaou M, El Hanaoui M, Yacoubi B, Moukrim A, Banaoui A (2022) Assessment of seasonal and spatial variation responses of integrated biomarkers in two marine sentinel bivalve species: Agadir Bay (Southern of Morocco). Mar Pollut Bull 174:113179. https://doi.org/10.1016/j.marpolbul.2021.113179

    Article  CAS  PubMed  Google Scholar 

  • Chromcova L, Blahova J, Zivna D, Plhalova L, Casuscelli F, Di Tocco L, Svobodova Z (2015) NeemAzal T/S-toxicity to early-life stages of common carp (Cyprinus carpio L.). Veterinární Medicína 60(1):23–30

    Article  CAS  Google Scholar 

  • Cossu C, Doyotte A, Jacquin MC, Babut M, Exinger A, Vasseur P (1997) Glutathione reductase, selenium-dependent glutathione peroxidase, glutathione levels, and lipid peroxidation in freshwater bivalves, Unio tumidus, as biomarkers of aquatic contamination in field studies. Ecotoxicol Environ Saf 38:122–131. https://doi.org/10.1006/eesa.1997.1582

    Article  CAS  PubMed  Google Scholar 

  • Dellali M, Romeo M, Gnassia-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. https://doi.org/10.1016/j.jembe.2004.12.020

    Article  CAS  Google Scholar 

  • Doran WJ, Cope WG, Rada RG, Sandheinrich MB (2001) Acetylcholinesterase inhibition in the three ridge mussel (Amblema plicata) by chlorpyrifos: implications for biomonitoring. Ecotoxicol Environ Saf 49:91–98. https://doi.org/10.1006/eesa.2000.2036

    Article  CAS  PubMed  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7(2):88–95

    Article  CAS  PubMed  Google Scholar 

  • El Mourabit Y, Agnaou M, Ait Alla A, Moukrim A (2022) Assessment of the marine ecotoxic state in the moroccan coastal area Anza-Taghazout following the installation of two wastewater treatment plants: a multibiomarker study using Mytilus galloprovincialis. Environ Sci Pollut Res 29:11718–11729. https://doi.org/10.1007/s11356-021-16046-z

    Article  CAS  Google Scholar 

  • Escartin E, Porte C (1997) The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environ Toxicol Chem 16:2090–2095. https://doi.org/10.1002/etc.5620161015

    Article  CAS  Google Scholar 

  • Fabrello J, Pagano M, Arrigo F, Ciscato M, Boldrin F, Giacobbe S, Matozzo V (2022) Identification of haemocytes and histological examination of gills of the spiny oyster Spondylus gaederopus (Linnaeus, 1758). Fish Shellfish Immunol 130:164–174

    Article  CAS  PubMed  Google Scholar 

  • Fisk AT, Hobson KA, Noratrom RJ (2001) Influence of chemical and biological factors on trophical transfer of persistent organic pollutants in northwater polynya marine food web. Environ Sci Technol 35:732–738. https://doi.org/10.1021/es001459w

    Article  ADS  CAS  PubMed  Google Scholar 

  • Flammarion P, Noury P, Garric J (2002) The measurement of cholinesterase activities as a biomarker in chub (Leuciscus cephalus): the Wsh length should not be ignored. Environ Pollut 120:325–333. https://doi.org/10.1016/S0269-7491(02)00137-9

    Article  CAS  PubMed  Google Scholar 

  • Forget J (1998) Impact neurotoxique de contaminants (pesticides et métaux) sur un crustacé marin Tigriopus brevicornis (Müller). Caractérisation de la cholinestérase et application à la surveillance des effets des polluants sur l'environnement marin. Thèse de Doctorat. Université de Paris 6. https://www.theses.fr/1998PA066491

  • Freitas R, Silvestro S, Coppola F, Meucci V, Battaglia F, Intorre L, Faggio C (2019) Biochemical and physiological responses induced in Mytilus galloprovincialis after a chronic exposure to salicylic acid. Aquat Toxicol 214:105258

    Article  CAS  PubMed  Google Scholar 

  • Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20(1):37–45. https://doi.org/10.1002/etc.5620200104

    Article  CAS  PubMed  Google Scholar 

  • Gagne F, Blaise C, Aoyama I, Luo R, Gagnon C, Couillard Y, Cambell P, Salazar M (2002) Biomarker study of a municipal effluent dispersion plume in two species of freshwater mussels. Environ Toxicol Chem 17(3):149–159. https://doi.org/10.1002/tox.10046

    Article  ADS  CAS  Google Scholar 

  • Galloway TS, Millward N, Browne MA, Depledge MH (2002) Rapid assessment of organophosphorous pesticide exposure using combined esterases as biomarkers. Aquat Toxicol 61:169–180. https://doi.org/10.1016/S0166-445X(02)00051-6

    Article  CAS  PubMed  Google Scholar 

  • George GS, Buchanan G (1990) Isolation, properties and induction of plaice liver cytosolic glutathione S-transferases. Fish Physiol Biochem 8(6):437–449. https://doi.org/10.1007/BF00003400

    Article  CAS  PubMed  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the frst enzymatic step in mercapturic acid formation. Biol Chem 249(22):7130–7139

    Article  CAS  Google Scholar 

  • Hamed HS, Ismal SM, Faggio C (2021) Effect of allicin on antioxidant defense system, and immune response after carbofuran exposure in Nile tilapia, Oreochromis niloticus. Comp Biochem Physiol C Toxicol Pharmacol 240:108919

    Article  CAS  PubMed  Google Scholar 

  • Hellou J, Yeats P, Steller S, Gagne F (2003) Chemical contaminants and biological indicators of mussel health during gametogenesis. Environ Toxicol Chem 22(9):2080–2087. https://doi.org/10.1897/02-396

    Article  CAS  PubMed  Google Scholar 

  • Hoarau P, Gnassia-Barelli M, Romeo M, Girard JP (2001) Differential induction of Glutathion S- Tranferases in the clam Ruditapes decussates exposed to organic compounds. Environ Toxicol Chem 20:141–147. https://doi.org/10.1897/02-396

    Article  Google Scholar 

  • Idardare Z, Chiffoleau JF, Moukrim A, Ait Alla A, Auger D, Lefrere L, Rozuel E (2008) Metal concentrations in sediment and Nereis diversicolor in two Moroccan lagoons: Khnifiss and Oualidia. Chem Ecol 24(5):329–340. https://doi.org/10.1080/02757540802378774

    Article  CAS  Google Scholar 

  • Impellitteri F, Multisanti CR, Rusanova P, Piccione G, Falco F, Faggio C (2023a) Exploring the impact of contaminants of emerging concern on fish and invertebrates physiology in the Mediterranean Sea. Biology 12(6):767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Impellitteri F, Yunko K, Martyniuk V, Matskiv T, Lechachenko S, Khoma V, Faggio C (2023b) Physiological and biochemical responses to caffeine and microplastics in Mytilus galloprovincialis. Sci Total Environ 890:164075

    Article  ADS  CAS  PubMed  Google Scholar 

  • Kaaya A, Najimi S, Ribera D, Narbonne JF, Moukrim A (1999) Characterization of glutathione S-transferases (GST) activities in Perna perna and Mytilus galloprovincialis used as a biomarker of pollution in the Agadir marine bay (South of Morocco). Bull Environ Contam Toxicol 62(5):623–629. https://doi.org/10.1007/s001289900920

    Article  CAS  PubMed  Google Scholar 

  • Khati W, Ouali K, Mouneyrac C, Banaoui A (2012) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use in biomonitoring. Energy Procedia 18:784–794. https://doi.org/10.1016/j.egypro.2012.05.094

    Article  CAS  Google Scholar 

  • Khessiba A, Hoarau P, Gnassia-Barelli M, Aissa P, Romeo M (2000) Biochemical responses of the mussel Mytilus galloprovincialis from Bizerta (Tunisia) exposed to chemical pollutants. Arch Environ Contam Toxicol 40:222–229. https://doi.org/10.1007/s002440010166

    Article  Google Scholar 

  • Kurt PB, Ozkoc HB (2004) A survey to determine levels of chlorinated pesticides and PCBs in mussels and seawater from the Mid-Black Sea Coast of Turkey. Mar Pollut Bull 48:1076–1083. https://doi.org/10.1016/j.marpolbul.2003.12.013

    Article  CAS  PubMed  Google Scholar 

  • Lagbouri A (1997) Etude de la biologie de Donax trunculus dans la baie d’Agadir et de la réponse à la pollution à travers trois biomarqueurs (acétylcholinestérase, péroxydation lipidique et Glutathion-S-Transférase). Thèse de 3ème cycle. Université Ibn Zohr. p 170, in Moukrim A, Kaaya, A, Najimi S, Romeo M, Gnassia-Barelli M, Narbonne J.F (2000) Assessment of the trace metal levels in two species of mussels from the Agadir Marine Bay, south of Morocco. Bull Environ Contam Toxicol 65:478–485. https://doi.org/10.1007/s001280000149

    Article  Google Scholar 

  • Laouati I, Rouane-Hacene O, Derbal F et al (2021) The mussel caging approach in the assessment of trace metal contamination in southern Mediterranean coastal waters: a multi-biomarker study. Environ Sci Pollut Res 28:63032–63044. https://doi.org/10.1007/s11356-021-15203-8

    Article  Google Scholar 

  • Li H, Jiang H, Gao X, Wang X, Qu W, Lin R, Chen J (2008) Acute toxicity of the Pesticide methomyl on the topmouthgudgeon (Pseudorasbora parva):mortality and effects on four biomarkers. Fish Physiol Biochem 34:209–216. https://doi.org/10.1007/s10695-007-9178-x

    Article  CAS  PubMed  Google Scholar 

  • Livingstone DR, Garcia-Martinez P, Michel X, Narbonne JF, O’Hara S, Ribera D, Winston G (1990) Oxyradical production as a pollution mediated mechanism of toxicity in the common mussel, Mytilus edulis and other molluscs. Funct Ecol 4:415–424

    Article  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein mea surement with the Folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  PubMed  Google Scholar 

  • Lubet P, Chappuis JG (1964) Study of water filtration in Mytilus, in Fiala-Médioni, A. Ethologie alimentaire d’invertébrés benthiques filtreurs (ascidies). I. Dispositif expérimental Taux de filtration et de digestion chez Phallusia mammillata. Mar Biol 23:137–145. https://doi.org/10.1007/BF00389171

    Article  Google Scholar 

  • Makaoui A, Orbi A, Aristegui J, Benazzouz A, Larissi J, Agouzouk A, Hilmi K (2012) Hydrological seasonality of cape Ghir. Nat Sci 4(1):5–13. https://doi.org/10.4236/ns.2012.41002

    Article  Google Scholar 

  • 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. https://doi.org/10.1016/j.aquatox.2004.07.003

    Article  CAS  PubMed  Google Scholar 

  • Marsh JB, Weinstein DB (1966) Simple charring method for determination of cal approach. Biomarkers 3:305–315

    Google Scholar 

  • Massoulié J, Bon S (1993) L’acétylcholinestérase : une structure originale pour une fonction vitale. Annales de l’Institut Pasteur/Actualités, 4(1):35–49. In: Tmimi FZ, Faraj C, Bkhache M et al (2018) Insecticide resistance and target site mutations (G119S ace-1 and L1014F kdr) of Culex pipiens in Morocco. Parasites Vect 11:51. https://doi.org/10.1186/s13071-018-2625-y

  • Matozzo V, Tomei A, Marin MG (2005) Acetylcholinesterase as a biomarker of exposure to neurotoxiccompounds in the clam Tapes philippinarum from the Lagoon of Venice. Mar Pollut Bull 50:1686–1693. https://doi.org/10.1016/j.marpolbul.2005.07.011

    Article  CAS  PubMed  Google Scholar 

  • Mehdaoui O, Fekhaoui M, descoins C (2000) Accumulation et biomagnification des insecticides organochlorés dans les mollusques et les poissons de la lagune de Moulay Bousselham, Au Maroc, Cahier santé 10:373–379. https://www.semanticscholar.org/paper/ca381370fb31289edd0ea343e07bd0cb77ba1dea

  • Menezes S, Soares AMVM, Guilhermino L, Peck M (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. https://doi.org/10.1016/j.jembe.2006.03.009

    Article  Google Scholar 

  • Mimouni R, Yacoubi B, Eddabra R (2011) Physicochemical quality of wastewater purified by infiltration-percolation: case of the plant of ben sergao (south-western morocco) after ten years of running. Rev Microbiol Ind San Environ 5(1):101–114

    Google Scholar 

  • Mora P, Fournier D, Narbonne JF (1999) Cholinesterases from the marine mussels Mytilus galloprovincialis Lmk. and M. edulis L. and from the freshwater bivalve Corbicula fluminea Muller. Comp Biochem Physiol C 122:353–361. https://doi.org/10.1016/S0742-8413(98)10130-5

    Article  CAS  PubMed  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 105:309–325. https://doi.org/10.1007/s10661-005-3854-z

    Article  CAS  PubMed  Google Scholar 

  • Moukrim A, Kaaya A, Najimi S, Romeo M, Gnassia-Barelli M, Narbonne JF (2000) Assessment of the trace metal levels in two species of mussels from the Agadir Marine Bay, south of Morocco. Bull Environ Contam Toxicol 65:478–485. https://doi.org/10.1007/s001280000149

    Article  CAS  PubMed  Google Scholar 

  • Moukrim A, El Hamidi F, Lagbouri A, Kaaya A, Zekhnini A, Bouhaimi A, Nar-bonne JF (2004) Donax trunculus as a sentinel species for environmental monitoring of sandy beaches on Moroccan coasts. Bull Environ Contam Toxicol 73:674–681. https://doi.org/10.1007/s00128-004-0479-9

    Article  CAS  PubMed  Google Scholar 

  • Multisanti CR, Merola C, Perugini M, Aliko V, Faggio C (2022) Sentinel species selection for monitoring microplastic pollution: a review on one health approach. Ecol Ind 145:109587

    Article  CAS  Google Scholar 

  • Najimi S, Bouhaimi A, Daubeze M, Zekhnini A, Pellerin J, Narbonne JF, Moukrim A (1997) Use of acetylcholinesterase in Pernaperna and Mytilus galloprovincialis as a biomarker of pollution in Agadir Marine Bay (south of Morocco). Bull Environ Contam Toxicol 58:901–908

    Article  CAS  PubMed  Google Scholar 

  • Narbonne JF, Garrigues P, Ribera D, Raoux C, Mathieu A, Lemaire AI, Salaün JP, Lafaurie M (1991) Mixed- function oxygenase enzymes as tools for pollution monitoring: Field studies on the French coasts of the mediterranean sea. Comp Biochem Physiol 100C:37–42. https://doi.org/10.1016/0742-8413(91)90118-D

    Article  CAS  Google Scholar 

  • Otchere FA (2005) Organochlorines (PCBs and pesticides) in the bivalves Anadara (Senilis) senilis, Crassostrea tulipa and Perna perna from the lagoons of Ghana. Sci Total Environ 348:102–114. https://doi.org/10.1016/j.scitotenv.2004.12.069

    Article  ADS  CAS  PubMed  Google Scholar 

  • Pagano M, Stara A, Aliko V, Faggio C (2020) Impact of neonicotinoids to aquatic invertebrates in vitro studies on Mytilus galloprovincialis: a review. J Mar Sci Eng 8(10):801

    Article  Google Scholar 

  • Pagano M, Fabrello J, Multisanti CR, Zicarelli G, Ciscato M, Boldrin F, Faggio C (2023) A first insight into haemocytes of Pinctada imbricata radiata: a morpho-functional characterization. Microsc Res Tech 86(3):368–377

    Article  CAS  PubMed  Google Scholar 

  • Pastor D, Sanpera C, Gonzalez-Solis J, Ruiz X, Albaiges J (2004) Factors affecting the organochlorine pollutant load in biota of a rice field ecosystem (Ebro Delta NE Spain). Chemosphere 55:567–576. https://doi.org/10.1016/j.chemosphere.2003.11.036

    Article  ADS  CAS  PubMed  Google Scholar 

  • Perez-Ruzafa V, Navarro S, Barba A, Marcos C, Camara MA, Salas F, Gltierrez JM (2000) Presence of pesticides throughout trophic compartments of the food web in the Mar Menor Lagoon (SE Spain). Mar Pollut Bull 40(2):140–151. https://doi.org/10.1016/S0025-326X(99)00193-9

    Article  CAS  Google Scholar 

  • Pfeifer S, Schiedek D, Dippner JW (2005) Effect of temperature and salinity on acetylcholinesterase activity, a common pollution bio marker, in Mytilus sp. from the south-western Baltic Sea. J Exp Mar Biol Ecol 320(1):93–103. https://doi.org/10.1016/j.jembe.2004.12.020

    Article  CAS  Google Scholar 

  • Pikkarainen AL (2007) Polychlorinated biphenyls and organochlorine pesticides in Baltic Sea sediments and bivalves. Chemosphere 68:17–24. https://doi.org/10.1016/j.chemosphere.2006.12.079

    Article  ADS  CAS  PubMed  Google Scholar 

  • Plhalova L, Blahova J, Divisova L, Enevova V, Casuscelli di Tocco F, Faggio C, Svobodova Z (2018) The effects of subchronic exposure to NeemAzal T/S on zebrafish (Danio rerio). Chem Ecol 34(3):199–210

    Article  CAS  Google Scholar 

  • Radenac G, Bocquene G, Fichet D, Miramand P (1998) Contamination of a dredged material disposal site (La Rochelle Bay, France). The use of the acetylcholinesterase activity of Mytilus edulis (L.) as a biomarker of pesticides: the need for a critical approach. Biomarkers. https://doi.org/10.1080/135475098231110

    Article  Google Scholar 

  • Rendón-von Osten J, Ortíz-Arana A, Guilhermino L, Soares AMVM (2005) In vivo evaluation of three biomarkers in the mosquitofish (Gambusia yucatana) exposed to pesticides. Chemosphere 58:627–636. https://doi.org/10.1016/j.chemosphere.2004.08.065

    Article  ADS  CAS  PubMed  Google Scholar 

  • Richardson BJ, Mak E, De Luca-Abbott SB, Martin M, McClellan K, Lam PKS (2008) Antioxidant responses to polycyclic aromatic hydrocarbons and organochlorine pesticides in green-lipped mussels (Perna viridis ): do mussels ‘‘integrate” biomarker responses? Mar Pollut Bull 57:503–514. https://doi.org/10.1016/j.marpolbul.2008.02.032

    Article  CAS  PubMed  Google Scholar 

  • Riley JP, Skirrow G (1975) Chemical oceanography, v. 4, 2nd edn. Academic Press, New York, p Xviii. https://doi.org/10.4319/lo.1976.21.5.0766

    Book  Google Scholar 

  • Robillard S, Beauchamp G, Laulier M (2003) The role of abiotic factors and pesticide levels on enzymatic activity in the freshwater mussel Anodonta cygnea at three different exposure sites. Comp Biochem Physiol Part C 135:49–59. https://doi.org/10.1016/S1532-0456(03)00049-8

    Article  CAS  Google Scholar 

  • Sharma S, Dar OI, Singh K, Kaur A, Faggio C (2021) Triclosan elicited biochemical and transcriptomic alterations in Labeo rohita larvae. Environ Toxicol Pharmacol 88:103748

    Article  CAS  PubMed  Google Scholar 

  • Sheehan D, Power A (1999) Effects of seasonality on xenobiotic and antioxidant defence mechanism of bivalve molluscs. Comp Biochem Physiol 123(C):193–199. https://doi.org/10.1016/S0742-8413(99)00033-X

    Article  CAS  Google Scholar 

  • Shiry N, Derakhshesh N, Alavinia SJ, Pouladi M, Falco F, Faggio C (2023) Anodonta cygnea, a freshwater swan mussel, exposed to diazinon: toxicity thresholds in behaviour and physiology. Vet Res Commun 47:1303–1319

    Article  PubMed  Google Scholar 

  • Solé M, Porte S, Barcelo D, Albaiges J (2000) Bivalves residue analysis for the assessment of coastal pollution in the Ebro Delta (NW Mediterranean). Mar Pollut Bull 40(9):746–753. https://doi.org/10.1016/S0025-326X(00)00011-4

    Article  Google Scholar 

  • Stara A, Bellinvia R, Velisek J, Strouhova A, Kouba A, Faggio C (2019) Acute exposure of common yabby (Cherax destructor) to the neonicotinoid pesticide. Sci Total Environ 665:718–723

    Article  ADS  CAS  PubMed  Google Scholar 

  • Stara A, Pagano M, Capillo G, Fabrello J, Sandova M, Albano M, Faggio C (2020) Acute effects of neonicotinoid insecticides on Mytilus galloprovincialis: a case study with the active compound thiacloprid and the commercial formulation calypso 480 SC. Ecotoxicol Environ Saf 203:110980

    Article  CAS  PubMed  Google Scholar 

  • Stara A, Pagano M, Albano M, Savoca S, Di Bella G, Albergamo A, Faggio C (2021) Effects of long-term exposure of Mytilus galloprovincialis to thiacloprid: a multibiomarker approach. Environ Pollut 289:117892

    Article  CAS  PubMed  Google Scholar 

  • Stein X, Percic P, Gnassia-Barelli M, Romeo M, Lafaurie M (1998) Evaluation of biomarkers in caged fishes and mussels to asses the quality of waters in a bay of the NW Mediterranean sea. Environ Poll 99:111–117. https://doi.org/10.1016/S0269-7491(98)00013-X

    Article  Google Scholar 

  • Sula E, Aliko V, Barceló D, Faggio C (2020) Combined effects of moderate hypoxia, pesticides and PCBs upon crucian carp fish, Carassius carassius, from a freshwater lake-in situ ecophysiological approach. Aquat Toxicol 228:105644

    Article  CAS  PubMed  Google Scholar 

  • Tlili S, Minguez L, Giamberini L, Geffard A, Boussetta H, Mouneyrac C (2013) Assessment of the health status of Donax trunculus from the Gulf of Tunis using integrative biomarker indices. Ecol Indic 32:285–293. https://doi.org/10.1016/j.ecolind.2013.04.003

    Article  Google Scholar 

  • Tresnakova N, Famulari S, Zicarelli G, Impellitteri F, Pagano M, Presti G, Faggio C (2023a) Multi-characteristic toxicity of enantioselective chiral fungicide tebuconazole to a model organism Mediterranean mussel Mytilus galloprovincialis Lamarck, 1819 (Bivalve: Mytilidae). Sci Total Environ 862:160874

    Article  ADS  CAS  PubMed  Google Scholar 

  • Tresnakova N, Impellitteri F, Famulari S, Porretti M, Filice M, Caferro A, Faggio C (2023b) Fitness assessment of Mytilus galloprovincialis Lamarck, 1819 after exposure to herbicide metabolite propachlor ESA. Environ Pollut 331:121878

    Article  CAS  PubMed  Google Scholar 

  • UNEP/FAO/IOC/IAEA (1993) Guidelines for monitoring chemical contaminants in the sea using marine organisms. Reference Methods For Marine Pollution Studies No. 6, UNEP

  • Vos RME, Van Bladeren PJ (1990) Glutathione S-transferases in relation to their role in the biotransformation of xenobiotics. Chem Biol Interact 75:241–265. https://doi.org/10.1016/0009-2797(90)90069-Y

    Article  CAS  PubMed  Google Scholar 

  • Wagne MM, Sefrioui S, Dartige A, Ould Zamel ML, Tounkara HA, Mbengue B (2012) Etude des lipides totaux de la moule Perna perna de la baie du Lévrier, Mauritanie. J Sci Halieut Aquat 5:152–160

    Google Scholar 

  • Wan MT, Kuo JK, Buday C, Schroeder G, Van Aggelen G, Pasternak J (2005) Toxicity of a-, b-, (a+b)-endosulfan and their formulated and degradation products to Daphnia magna, Hyalella azteca, Oncorhynchus mykiss, Oncorhynchus kisutch, and biological implications in streams. Environ Toxicol Chem 24:1146–1154. https://doi.org/10.1897/04-300R1.1

    Article  CAS  PubMed  Google Scholar 

  • Wang C, Lu G, Cuib J, Wanga P (2009) Sublethal effects of pesticide mixtures on selected biomarkers of Carassius auratus. Environ Toxicol Pharmacol 28:414–419. https://doi.org/10.1016/j.etap.2009.07.005

    Article  CAS  PubMed  Google Scholar 

  • Yatawara M, Qi Sh, Owago OJ, DanYang YZ, ZhangBurnet JEJ (2010) Organochlorine pesticide and heavy metal residues in some edible biota collected from Quanzhou Bay and Xinghua Bay, Southeast China. J Environ Sci 22(2):314–320. https://doi.org/10.1016/S1001-0742(09)60110-8

    Article  CAS  Google Scholar 

  • Zhao Z, Zhang L, Wu J, Fan Ch (2009) Distribution and bioaccumulation of organochlorine pesticides in surface sediments and benthic organisms from Taihu Lake, China. Chemosphere 77:1191–1198. https://doi.org/10.1016/j.chemosphere.2009.09.022

    Article  ADS  CAS  PubMed  Google Scholar 

  • Zengeya T, Ivey P, Woodford DJ, Weyl O, Novoa A, Shackleton R, et al. (2017) Managing conflict-generating invasive species in South Africa: Challenges and trade-offs. Bothalia 47(2):a2160. https://doi.org/10.4102/abc.v47i2.2160

    Article  Google Scholar 

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Agnaou, M., Ait Alla, A., Nadir, M. et al. The use of brown mussel as bioindicator of pesticides pollution in Agadir Bay (Southern Morocco). Trop Ecol (2024). https://doi.org/10.1007/s42965-024-00325-0

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