Toxicity of a fungicide based on a copper oxychloride in the presence of cadmium on snail (Helix aspersa) biomarkers

Paper Details

Research Paper 01/04/2018
Views (461) Download (15)

Toxicity of a fungicide based on a copper oxychloride in the presence of cadmium on snail (Helix aspersa) biomarkers

Khadidja Farfar, Mohamed El Hadi Khebbeb, Mohamed Reda Djebar
J. Bio. Env. Sci.12( 4), 39-47, April 2018.
Certificate: JBES 2018 [Generate Certificate]


Considerable attention has been paid to the problem of soil contamination by heavy metals. Heavy metal pollutant toxicity to the environment has been gained from tests involving single pollutants. However, multiple metals commonly occur together and they may exert toxicity simultaneously. This work aim to evaluate the synergistic effect of Cadmium and a copper-based fungicide, on biomarker response of a gastropod, Helix aspersa. Cd and fungicide were ingested alone or mixed for 15, 30 and 90 days. After each period, Protein, Malonedialdehyde and Glutathione levels were measured in liver while acetylcholine esterase activity was assessed in brain. Obtained results showed that malonedialdehyde levels in the liver of treated snails increased compared to the corresponding control (from +66% to +230%). In addition, the highest increase was seen in snails treated with Cd + Fungicide (+330 and +230% at respectively day 30 and 90). Reduced glutathione content decreased in all treated groups (-34%, -25% and -22% at day 15, 30 and 90 for Cd and fungicide group) and the highest decrease (-43%) was observed at day 90 in snails treated with Cd + Fungicide. In addition, acetylcholine esterase activity also decreased in the three treatment groups (-13% to -63%) and the strongest decrease was seen in snails treated with Cd + Fungicide after 90 days (-63%). These results showed the appearance of oxidative stress, which was much more pronounced when the fungicide was combined with Cd. Based on these results, users of plant protection products are advised to be vigilant and cautious in order to avoid a possible cocktail effect.


Adam V, Zehnàlek J, Petrlovã J, Potešil D, Sures B, Trnkovà L, Jelen F, Viteeek J, Kizek R. 2005.Phytochelatin Modified Electrode Surface as a Sensitive Heavy- Metal Ion Biosensor.Sensors5, 70-84.

ATSDR(Agency for Toxic Substances and Disease Registry). 2004. Copper, CAS # 7440-50-8.

Banci L, Bertini I, Ciofi-Baffoni S, Hadjiloi T, Martinelli M, Palumaa P. 2008. Mitochondrial copper (I) transfer from Cox17 to Sco1 is coupled to electron transfer, Proceedings of the National Academy of Sciences 105 6803–6808.

Beldi H, Gimbert F, Maas S, Scheifler R, Soltani N. 2006. Seasonal variations of Cd, Cu, Pband Zn in the edible mollusc Donax trunculus (Mollusca, Bivalvia) from the gulf of Annaba, Algeria. African Journal of Agricultural Research 1(4), 85-90.

Bensouda L, Soltani-Mazouni N.2014. Measure of oxidative stress and neurotoxicity biomarkers in Donax trunculus from the Gulf of Annaba (Algeria): Case of the Year2012. Annual Research & Review in Biology 4(12),1902-1914.

Bouzenda R, Soltani N, Khebbeb MEH. 2017. Assessment of pollution in the Gulf of Annaba(Algeria) by monthly measurements of two biomarkers in a fish species Liza aurata. Journal of Entomology and Zoology Studies 5(1),366-372.

Bradford MM. 1976.A rapid and sensitive method for the quantification of microgram quantities of protein utilizingthe principle of protein-dye binding. Analytical Biochemistry 72,248-254.

CanesiL,Ciacci C, Piccoli G, Stocchi V, Viarengo A, Gallo G. 1998. In vitro and in vivo effects of heavy metals on mussel digestive gland hexokinase activity: the role of glutathione Comparative Biochemistry and Physiology 120, 261-268.

Cossu A, Doyotte M, Babut A, Exinger P. 2000.Antioxidant Biomarkers in Freshwater Bivalves, Uniotumidus, in Response to Different Contamination Profiles of Aquatic Sediments, Ecotoxicology Environmental Safety 45, 106-121.

Cravo A, Pereira C, Gomes T, Cardoso C, Serafim A, Almeida C. 2012.A multi-biomarker approach in the clam Ruditapes decussatus to assess the impact of pollution in the Ria Formoso lagoon. South Coast of Portugal. Marine Environmental Research 75, 23-34. 3

Dewes IJ, Sandrine JZ, Monserrat JM, Yunes JS. 2006. Biochemical and physiological responses after exposure to microcystins in the crab Chasmagnathus granulatus (Decapoda, Brachyura). Ecotoxicology and Environmental Safety 65,201-208.

Draper HH, Hadley M. 1990. Malondialdehyde determination as index of lipid Peroxidation Methods in Enzymology 1990, 186, 421-431.

Ellman GL, Courtney KD, Andreas V, Featherstone RM. 1961. A new and rapid colorimetric determination of AChE activity. Biochemistry and Pharmacology 7,88-95.

Führer E, Rudolph A, Espinoza C, Díaz R, Gajardo M, Camano N.2012. Integrated use of biomarkers (O:n ratio and acetylcholinesterase inhibition) on Aulacomyater (Molina, 1782) (Bivalvia: Mytilidae) as a criteria for effects of organophosphate pesticide exposition. Hindawi Publishing Corporation. Journal of Toxicology Article ID 951568, 6 pages

Geret F, Jouan A, Tupin V, Bebianno MJ, Cosson RP.2002. Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalve mollusks: the oyster (Crassostrea gigas) and the mussel (Mytilusedulis). Aquatic Living Resources 15, 61-66.

Giguère Y, Couillard, PGC, Campbell O, Perceval L, Hare B, Pinel-Alloul J, Pellerin J. 2003.Steady-state distribution of metals among metallothionein and other cytosolic ligands and links to cytotoxicity in bivalves living along a polymetallic gradient. Aquatic Toxicology 64, 185–200.

Gimbert F, de Vaufleury A, Douay F, Coeurdassier M, Scheifler R, Badot PM. 2006. Modelling chronic exposure to contaminated soil: a toxicokinetic approach with the terrestrial snail Helixaspersa. Environment International 32, 866-875.

Hamza-Chaffai J, Pellerin J, Amiard C. 2003.Health assessment of a marine bivalve Ruditapes decussatus from the Gulf of Gabès (Tunisia).Environment International 28, 609–617.

Jebali J, Ben-Khedher S, Ghedira J, Kamel N, Boussetta H.2011. Integrated assessment of biochemical responses in Mediterranean crab (Carcinus maenas) collected from Monastir Bay Tunisia. Journal of Environmental Science 23(10),1714-1720.

Khebbeb MEH, 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). Annals of Biological Research 1(2),166-173.

Larba R, Soltani N.2014. Use of the land snail Helix aspersa for monitoring heavy metal soil contamination in Northeast Algeria. Environmental Monitoring and Assessment 186(8),4987-4995.

Larbaa R, Soltani N. 2013. Diversity of the terrestrial gastropods in the Northeast Algeria: Spatial and temporal distribution. European Journal of Experimental Biology 3(4), 209-215.

Li GH, Cao ZM, Lan DZ, Xu J, Wang SS, Yin WH. 2007. Spatial variations in grain size distribution and selected metal contents in the Xiamen Bay, China.Environmental Geology 52,1559- 1567.

Machreki-Ajmi M, Ketata I, Ladhar-Chaabouni R, Hamza-Chaffai A.2008.The effect of in situ cadmium contamination on some biomarkers in Cerastoderma glaucum. Ecotoxicology 17, 1–11

Masaya M, Yoshinobu H, Ai Y, Maki K, Yasuo O.2002.Determination of cellular levels of non protein thiols in phytoplankton and their correlations with susceptibility to mercury1.Journal of Phycology 38(5).

Pyatt AJ, Pyatt FB, Pentreath VW. 2002. Lead toxicity, locomotion and feeding in the freshwater snail, Lymnaea stagnalis (L.), Invertebrate Neurosciences 4,135–140.

Qian H, Li J, Pan X, Sun L, Lu T, Ran H, Fu Z.2011. Combined Effect of Copper and Cadmium on Heavy Metal Ion Bioaccumulation and Antioxidant Enzymes Induction in Chlorella vulgaris. Bulletin of Environmental Contamination and Toxicology 87,512–516.

Ringwood AH, Conner DF, Keppler CJ, AA. Dinovo AA. 1999. Biomarker studies with juvenile oysters (Crassostrea virginica) deployed in-situ Biomarkers4, 400 – 414.

Roméo M, Gnassia-Barelli M. 1997. Effect of Heavy Metals on Lipid Peroxidation in the Mediterranean Clam Ruditapes decussatus Comparative Biochemistry and Physiology 118, 33-37.

Scheifler R, Gomot A, de Vauflenry A, Badot PM. 2002. Transfer of cadmium from plant leaves and vegetable flour to the snail Helix aspersa: bioaccumulation and effects. Ecotoxicology and Environmental Safety 53, 148–153.

Sebbio C, Carere C, Nascetti G, Bellisario B, Mosesso P, Cimmaruta R, Angeletti D. 2014. Interspecies variation in DNA damage induced by pollution. Current Zoology 60, 308–314.

Serafim A, Lopes B, Company R, Cravo A, Gomes T, Soussa V. 2011. A multi-biomarker approach in cross transplanted mussels Mytilus galloprovincialis. Ecotoxicology 20,1959-1974.

Sies H. 1999.Glutathione and its role in cellular functions. Free Radical Biology and Medecine27, 916-921.

Soltani N, Amira N, Sifi K, Beldi H.2012. Environmental monitoring of the Annaba Gulf (Algeria):Measurement of biomarkers in Donax trunculus and metallic pollution. Bulletin de la Société Zoologique de France 137(1-4),51-60.

Sureda A, Box M, Enseñat E, Alou P, Tauler S, Deudero A. Pons. 2006. Enzymatic antioxidant response of a labrid fish (Corisjulis) liver to environmental caulerpenyne. Comparative Biochemistry and Physiology 144, 191-196.

Tim-Tim ALS, Margado F, Moreira S, Rangel R, Nogueira AJA, Soares AMVM. 2009. Cholinesterase and glutathione S-transferase activities of three mollusc species from the NW Portuguese Coast in the relation tothe «Prestige» oil spill. Chemosphere 77,1465- 1475.

Tlili S, Metais I, Boussetta H, Louneyrac C.2010. Linking changes at sub-individual and population levels in Donax trunculus: Assessment of marine stress. Chemosphere 81, 692-700.

Tlili S, Minguezc L, Giamberinic L, Geffard A, Boussetta H, Mouneyraca C. 2013.Assessment of the health status of Donax trunculus from the Gulf of Tunis using integrative biomarker indices. Ecological Indicators 32,285-293.

Viarengo L, Canesi M, Pertica G, Poli MN, Moore M, Orunesay M. 1990. Heavy metal effects on lipid peroxidation in the tissues of mytilus galloprovincialis lam. Comparative Biochemistry and Physiology 97, 37-42.

Wang Z, Yan C, Zhang X.2009.Acute and chronic cadmium toxicity to a saltwater cladoceran Moinamonogolica Daday and its relative importance. Ecotoxicology 18, 47–54.

Weckberker G, Cory G.1988. Ribonucleotide reductase activity and growth of glutathione-depleted mouse leukemia L1210 cells in vitro. Cancer letters 40, 257-264.

Yu BP.1994.Cellular defenses against damage from reactive oxygen species. Physiological Reviews, 74, 139-162.