Abstract
The aim of this investigation was to identify major pesticides that may cause detrimental effects in bivalve species affected by agricultural pollution. Investigations were carried out using freshwater clams (Corbicula fluminea) transplanted in the main drainage channels that collect the effluents coming from agriculture fields in the Ebro Delta (NE Spain) during the main growing season of rice (from May to August). Environmental hazards were assessed by measuring simultaneous up 46 contaminant levels and 9 biomarker responses. Measured biological responses showed marked differences across sites and months. Antioxidant and esterase enzyme responses were in most cases inhibited. Lipid peroxidation levels increased steadily from May in upstream stations to August in drainage channels. Principal Component (PCA) and Partial Least Squares to Latent Structure regression (PLS) analyses allowed the identification of endosulfan, propanil, and phenylureas as being the chemical contaminants causing the most adverse effects in the studied species.
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References
Angelo RT, Cringan MS, Chamberlain DL, Stahl AJ, Haslouer SG, Goodrich CA (2007) Residual effects of lead and zinc mining on freshwater mussels in the Spring River Basin (Kansas, Missouri, and Oklahoma, USA). Sci Tot Environ 384:467–496
Barata C, Lekumberri I, Vila-Escalé M, Prat N, Porte C (2005) Trace metal concentration, antioxidant enzyme activities and susceptibility to oxidative stress in the tricoptera larvae Hydropsyche exocellata from the Llobregat riven basin (NE Spain). Aquat Toxicol 74:3–19
Barata C, Damásio J, López MA, Kuster M, De Alda ML, Barcelo D, Riva MC, Raldúa D (2007) Combined use of biomarkers and in situ bioassays in Daphnia magna to monitor environmental hazards of pesticides in the field. Environ Toxicol Chem 26:370–379
Binelli A, Riva C, Provin A (2007) Biomarkers in Zebra mussel for monitoring and quality assessment of Lake Maggiore (Italy). Biomarkers 12:349–368
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dyebinding. Anal Biochem 72:248–254
Carrasco L, Díez S, Soto DX, Catalan J, Bayona JM (2008) Assessment of mercury and methylmercury pollution with zebra mussel (Dreissena polymorpha) in the Ebro River (NE Spain) impacted by industrial hazardous dumps. Sci Tot Environ 407:178–184
Damásio J, Tauler R, Teixidó E, Rieradevall M, Prat N, Riva MC, Soares AMVM, Barata C (2008) Combined use of Daphnia magna in situ bioassays, biomarkers and biological indices to diagnose and identify environmental pressures on invertebrate communities in two Mediterranean urbanized and industrialized rivers (NE Spain). Aquat Toxicol 87:310–320
Doherty FG (1990) The Asiatic clam, Corbicula sp, as a biological monitor in freshwater environments. Environ Monitor Assess 15:143–181
Escartín E, Porte C (1997) The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environ Toxicol Chem 16:2090–2095
Faria M, Carrasco L, Diez S, Riva MC, Bayona JM, Barata C (2009) Multi-biomarker responses in the freshwater mussel Dreissena polymorpha exposed to polychlorobiphenyls and metals. Comp Biochem Physiol 149C:281–288
Fatima M, Mandiki SNM, Douxfils J, Silvestre F, Coppe P, Kestemont P (2007) Combined effects of herbicides on biomarkers reflecting immune–endocrine interactions in goldfish immune and antioxidant effects. Aquat Toxicol 81:159–167
Feldman KL, Armstrong DA, Dumbauld BR, DeWitt TH, Doty DC (2000) Oysters, crabs, and burrowing shrimp: review of an environmental conflict over aquatic resources and pesticide use in Washington State’s (USA) coastal estuaries. Estuaries 23:141–176
Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, Oxford
Jolliffe IT (2002) Principal component analysis. Springer, Berlin
Kuster M, López de Alda MJ, Barata C, Raldúa D, Barceló D (2008) Analysis of 17 polar to semi-polar pesticides in the Ebro river delta during the main growing season of rice by automated on-line solid-phase extraction-liquid chromatography-tandem mass spectrometry. Talanta 75:390–401
Lacorte S, Raldúa D, Martínez E, Navarro A, Diez S, Bayona JM, Barceló D (2006) Pilot survey of a broad range of priority pollutants in sediment and fish from the Ebro river basin (NE Spain). Environ Pollut 140:471–482
Livingstone DR (2001) Contaminated-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666
Mañosa S, Mateo R, Guitart R (2001) A review of the effects of agricultural and industrial contamination on the Ebro delta biota and wildlife. Environ Monit Assess 71:187–205
Matozzo V, Ballarin L, Marin MG (2004) Exposure of the clam Tapes philippinarum to 4-nonylphenol: changes in anti-oxidant enzyme activities and re-burrowing capability. Mar Pollut Bull 48:563–571
Mora P, Michel X, Narbonne JF (1999) Cholinesterase activity as potential biomarker in two bivalves. Environ Toxicol Pharmacol 7:253–260
Moraes BS, Loro VL, Glusczak L, Pretto A, Menezes C, Marchezan E, de Oliveira Machado S (2007) Effects of four rice herbicides on some metabolic and toxicology parameters of teleost fish (Leporinus obtusidens). Chemosphere 68:1597–1601
Morcillo Y, Albalat A, Porte C (1999) Mussels as sentinels of organotin pollution: bioaccumulation and effects on P450-mediated aromatase activity. Environ Toxicol Chem 18:1203–1208
Oros DR, Ross JRM (2005) Polycyclic aromatic hydrocarbons in bivalves from the San Francisco estuary: spatial distributions, temporal trends, and sources (1993–2001). Mar Environ Res 60:466–488
Peña-Llopis S, Ferrando MD, Peña JB (2002) Impaired glutathione redox status is associated with decreased survival in two organophosphate-poisoned marine bivalves. Chemosphere 47:485–497
Porte C, Solé M, Borghi V, Martinez M, Chamorro J, Torreblanca A, Ortiz M, Orbea A, Soto M, Cajaraville MP (2001) Chemical, biochemical and cellular responses in the digestive gland of the mussel Mytilus galloprovincialis from the Spanish Mediterranean coast. Biomarkers 6:335–350
Ramón M, Cano J, Peña JB, Campos MJ (2005) Current status and perspectives of mollusc (bivalves and gastropods) culture in the Spanish Mediterranean. Boletín Instituto Español de Oceagografía 2:361–373
Santos TCR, Rocha JC, Barceló D (2000) Determination of rice herbicides, their transformation products and clofibric acid using on-line solid-phase extraction followed by liquid chromatography with diode array and atmospheric pressure chemical ionization mass spectrometric detection. J Chromatogr A 879:3–12
Solé M, Porte C, Albaigés J (1994) Mixed-function oxygenase system components and antioxidant enzymes in different marine bivalves: its relation with contaminant body burdens. Aquat Toxicol 30:271–283
Solé M, Porte C, Barceló D, Albaigés J (2000) Bivalves residue analysis for the assessment of coastal pollution in the Ebro Delta (NW Mediterranean). Mar Pollut Bull 40:746–753
Terrado M, Kuster M, Raldúa D, Lopez De Alda M, Barceló D, Tauler R (2007) Use of chemometric and geostatistical methods to evaluate pesticide pollution in the irrigation and drainage channels of the Ebro river delta during the rice-growing season. Anal Bioanal Chem 387:1479–1488
Vandeginste BGM, Massart DL (1998) Handbook of chemometrics and qualimetrics. Elsevier, Amsterdam
Vidal ML, Bassères A, Narbonne JF (2002a) Seasonal variations of pollution biomarkers in two populations of Corbicula fluminea. Comp Biochem Physiol 131C:133–151
Vidal ML, Bassères A, Narbonne JF (2002b) Influence of temperature, pH, oxygenation, water-type and substrate on biomarker responses in the freshwater clam Corbicula fluminea. Comp Biochem Physiol 132C:93–104
Wold S, Jonsson J, Sjostrom M, Sandberg M, Rannar S (1993) DNA and peptide sequences and chemical processes multivariately modelled by principal component analysis and partial least-squares projections to latent structures. Anal Chim Acta 277:239–253
Wold S, Sjostrom M, Eriksson L (2001) PLS-regression: a basic tool of chemometrics. Chem Sci Technol Lab 58:109–130
Zar JH (1996) Bioestatistical analysis. Bioestatistical AnalysisPrentice-Hall International, Inc, New Jersey
Acknowledgments
This study was partially supported by the European Union project “Integrated modeling of the river-sediments-soil-groundwater system; advanced tools for the management of catchment areas and river basins in the context of global change” [AQUATERRA], the Spanish Ministry of Education and Science projects [CGL2004-03514/HD; CGL2007-64551/HID; CTM2007-62436], and by the FCT Project PTDC/BIA-BDE/72841/2006. Joana Damásio was supported by an FCT PhD grant (SFRH/BD/23269/2005).
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Damásio, J., Navarro-Ortega, A., Tauler, R. et al. Identifying major pesticides affecting bivalve species exposed to agricultural pollution using multi-biomarker and multivariate methods. Ecotoxicology 19, 1084–1094 (2010). https://doi.org/10.1007/s10646-010-0490-3
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DOI: https://doi.org/10.1007/s10646-010-0490-3