Abstract
This study evaluated the toxicity of pesticide formulations Kraft® 36 EC (active ingredient—a.i. abamectin) and Score® 250 EC (a.i. difenoconazole), and their mixtures in Daphnia magna at different biological levels of organization. Survival, reproduction and biochemical markers (cholinesterase (ChE), catalase (CAT) and lipid peroxidation (LPO)) were some of the endpoints evaluated. Total proteins and lipids were also studied together with energy consumption (Ec). D. magna neonates were exposed for 96 h to Kraft (2, 4, and 6 ng a.i./L) and Score (12.5, 25, and 50 µg a.i./L) for the biochemical experiments, and for 15 days to abamectin (1–5 ng a.i./L) and to difenoconazole (3.12–50 µg a.i./L) to assess possible changes in reproduction. Exposures of organisms to both single compounds did not cause effects to antioxidant and detoxifying enzymes, except for LPO occurring at the highest concentration of difenoconazole tested. For ChE and CAT there was enzymatic induction in mixture treatments organisms, occurring at minor pesticides concentrations for CAT and at the two highest concentrations for ChE. There were no significant differences for total protein in D. magna but lipids showed an increase at the highest concentrations of pesticide mixture combinations. There was a significant increase of Ec in individuals of all treatments tested. In the chronic test, increased fecundity occurred for D. magna under difenoconazole exposures and mixtures. This study demonstrated that mixtures of these pesticides caused greater toxicity to D. magna than when tested individually, except for Ec. Therefore, effects of mixtures are very hard to predict only based on information from single compounds, which most possibly is the result of biological complexity and redundancy in response pathways, which need further experimentation to become better known.
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References
Aebi H (1984) Catalase in vitro. Meth Enzyme 105:121–126
Afiyanti M, Chen HJ (2014) Catalase activity is modulated by calcium and calmodulin in detached mature leaves of sweet potato. J Plant Physiol 171:35–47
Ahmad I, Pacheco M, Santos MA (2004) Enzymatic and nonenzymatic antioxidants as an adaptation to phagocyte-induced damage in Anguilla anguilla L. following in situ harbor water exposure. Ecotox Environ Safe 57:290–302
Albuquerque AF, Ribeiro JS, Kummrow F, Nogueira AJA, Montagner CC, Umbuzeiro GA (2016) Pesticides in Brazilian freshwaters: a critical review. Environ Sci Processes Impacts 18:779–787
Ali A, Xue RD, Alam SK (1997) Ecotoxicological effects of abamectin (MK-936) on natural populations of selected invertebrates in man-made ponds. Med Entomol Zool 48:233–241
Andrade TS, Henriques JF, Almeida AR, Machado AL, Koba O, Giang PT, Soares AM, Domingues I (2016) Carbendazim exposure induces developmental, biochemical and behavioural disturbance in zebrafish embryos. Aquat Toxicol 170:390–399
Araujo GS, Pinheiro C, Pestanaa JLT, Soares AMVM, Abessa DMS, Loureiro S (2019) Toxicity of lead and mancozeb differs in two monophyletic Daphnia species. Ecotoxicol Environ Saf 178:230–238
American Society for Testing and Materials (ASTM) (1980) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. American Society for Testing and Materials, Philadelphia, USA, pp. 729–780, Report E729-80.
Baird DJ, Barber I, Bradley MC, Calow P, Soares AMVM (1989) The Daphnia bioassay: a critique. Hydrobiologia 188:403–406
Barata C, Solayan A, Porte C (2004) Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquat Toxicol 66:125–139
Barata C, Varo I, Navarro JC, Arun S, Porte C (2005) Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol. Toxicol Pharmacol: CBP 140:175–186
Bird RP, Draper HH (1984) Comparative studies on different methods of malonaldehyde determination. Methods Enzymol 105:299–305
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein, utilising the principle of protein-dye landing. Anal Biochem 72:248–254
Brown PJ, Long SM, Spurgeon DJ, Svendsen C, Hankard PK (2004) Toxicological and biochemical responses of the earthworm Lumbricus rubellus to pyrene, a non-carcinogenic polycyclic aromatic hydrocarbon. Chemosphere 57:1675–81
Calabrese EJ, Baldwin LA (2002) Defining hormesis. Hum Exp Toxicol 21(2):91–97
Calabrese EJ, Baldwin LA (2003) Inorganics and hormesis. Crit Rev Toxicol 33:215–304
Campbell WC (1989) Ivermectin and Abamectin. Springer Verlag, New York, NY
Casali-Pereira MP, Daam MA, Resende JC, Vasconcelos AM, Espíndola EL, Botta CM (2015) Toxicity of Vertimec®18 EC (active ingredient abamectin) to the neotropical cladoceran Ceriodaphnia silvestrii. Chemosphere 139:558–564
Cedergreen N, Svendsen C, Backhaus T (2013) Toxicity prediction of chemical mixtures. Encyclopedia of Environmental Management. Vol null. Taylorand Francis, New York, pp 2572–2581. https://doi.org/10.1081/E-EEM-120046684
Cedergreen N, Kudsk P, Mathiassen SK, Sorensen H, Streibig JC (2007) Reproducibility of binary-mixture toxicity studies. Environ Toxicol Chem 26:149–156
Cheminova (2019) Freely accessible via http://www.adapar.pr.gov.br/arquivos/File/defis/DFI/Bulas/Inseticidas/kraft.pdf (Accessed 22 Nov 2019)
Coelho S, Oliveira R, Pereira S, Musso C, Domingues I, Bhujel RC, Soares AMVM, Nogueira AJA (2011) Assessing lethal and sub-lethal effects of trichlorfon on different trophic levels. Aquat Toxicol 103:191–198
Coors A, Frische T (2011) Predicting the aquatic toxicity of commercial pesticides mixtures. Environ Sci Europe 23/22:1–18
Cox C, Surgan M (2006) Unidentified inert ingredients in pesticides: implicationsfor human and environmental health. Environ Health Perspect 114:1803–1806
Day KE, Scott IM (1990) Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides. Aquat Toxicol 18:101–113
De Coen WM, Janssen CR (1997) The use of biomarkers in Daphnia magna toxicity testing. IV. Cellular Energy Allocation: a new methodology to assess the energy budget of toxicant-stressed Daphnia population. J Aquat Ecosyst Stress Recov 6:43–55
De Coen WM, Janssen CR (2003) The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics. Environ Toxicol Chem 22:1632–1641
Deneer JW (2000) Toxicity of mixtures of pesticides in aquatic systems. Pest Manag Sci 56:516–520
European Commission (EC) (2006a) Draft Assessment Report (DAR) – Public version-Initial risk assessment provided by the Rapporteur Member State theNetherlands for the existing active substance abamectin of the third stage (PartA) of the review programme referred to in Article 8(2) of Council Directive91/414/EEC
European Commission (EC) (2006b) Draft Assessment Report (DAR) – Public version– Initial risk assessment provided by the Rapporteur Member State Sweden forthe existing active substance difenoconazole of the third stage (Part A) of thereview programme referred to in Article 8(2) of Council Directive 91/414/EEC
European Food Safety Authority (EFSA) (2008) Conclusion regarding the peer review of the pesticide risk assessment of the active substance abamectin. EFSA J 147:1–106
European Food Safety Authority (EFSA) (2011) Conclusion on the peer review of the pesticide risk assessment of the active substance difenoconazole. EFSA J 9(1):1967
Ellman GL, Diane Courtney K, Andres Jr V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Ferreira NG, Morgado R, Santos MJ, Soares AMVM, Loureiro S (2015) Biomarkers and energy reserves in the isopod Porcellionides pruinosus: the effects of long-term exposure to dimethoate. Sci Total Environ 502:91–102
Ferrario C, Parolini CM, De Felice B, Villa S, Finizio A (2018) Linking sub-individual and supra-individual effects in Daphnia magna exposed to sub-lethal concentration of chlorpyrifos. Environ Poll 235:411–418
Figueirêdo LP, Daam MA, Mainardi G, Mariën J, Espíndola ELG, van Gestel CAM, Roelofs D (2019) The use of gene expression to unravel the single and mixture toxicity of abamectin and difenoconazole on survival and reproduction of the springtail Folsomia candida. Environ Poll 244:342–350
Forbes VE (2000) Is hormesis an evolutionary expectation? Funct Ecol 14:12–24
Freitas EC, Rocha O (2012) Acute and chronic effects of atrazine and sodium dodecyl sulfate on the tropical freshwater cladoceran Pseudosida ramosa. Ecotoxicology 21(5):1347–1357
García-Esquivel Z, Bricelj VM, Felbeck H (2002) Metabolic depression and whole-body response to enforced starvation by Crassostrea gigas postlarvae. Comp Biochem Physiol A 133:63–77
Gottardi M, Birch MR, Dalhoff K, Cedergreen N (2017) The effects of epoxiconazole and α-cypermethrin on Daphnia magna growth, reproduction and offspring size. Environ Toxicol Chem 36(8):2155–2166
Goulden CE, Henry L, Berrigan D (1987) Egg size, postembryonic yolk, and survival ability. Oecologia 72(1):28–31
Guilhermino L, Lopes MC, Carvalho AP, Soares AM (1996) Acetylcholinesterase activity in juveniles of Daphnia magna Straus. Bull Environ Contam Toxicol 57:979–985
Hassold E, Backhaus T (2014) The predictability of mixture toxicity of demethylase inhibiting fungicides to Daphnia magna depends on life-cycle parameters. Aquat Toxicol 152:205–214
Holth TF, Nourizadeh-Lillabadi R, Blaesbjerg M, Grung M, Holbech H, Petersen GI, Aleström P, Hylland KA (2008) Differential gene expression and biomarkers in zebrafish (Danio rerio) following exposure to produced water components. Aquat Toxicol 90:277–291
Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotox Environ Safe 54:366–374
Insecticide Resistance Action Committee (IRAC) (2019) IRAC MoA Classification Scheme, version 8.1. Freely available via: http://www.irac-online.org/documents/moa-classification/ (Accessed 19 Nov 2019)
Jager T, Barsi A, Ducrot V (2013) Hormesis on life-history traits: is there such thing as a free lunch? Ecotoxicology 22(2):263–270
Jemec A, Drobne D, Tisler T, Trebse P, Ros M, Sepcic K (2007) The applicability of acetylcholinesterase and glutathione S-transferase in Daphnia magna toxicity test. Comparative biochemistry and physiology. Toxicol & Pharmacol: CBP 144:303–309
Jeon J, Kretschmann A, Escher BI, Hollender J (2013) Characterization of acetylcholinesterase inhibition and energy allocation in Daphnia magna exposed to carbaryl. Ecotoxicol Environ Saf 98:28–35
Jiang H, Zhang XJ (2008) Acetylcholinesterase and apoptosis. A novel perspective for an old enzyme. FEBS J 275:612–617
Johnson RM, Dahlgren L, Siegfried BD, Ellis MD (2013) Acaricide, fungicideand drug interactions in honey bees (Apis mellifera). PLoS ONE 8:e54092
Junghans M, Backhaus T, Faust M, Scholze M, Grimme LH (2006) Application and validation of approaches for the predictive hazard assessment of realistic pesticide mixtures. Aquat Toxicol 76:93–110
Kim HY, Yu S, Jeong TY, Kim SD (2014) Relationship between trans-generational effects of tetracycline on Daphnia magna at the physiological and whole organism level. Environ Pollut 191:111–118
Kroon FJ, Hook SE, Metcalfe S, Jones D (2015) Altered levels of endocrine biomarkers in juvenile barramundi, Lates calcarifer (Bloch), following exposure to commercial herbicide and surfactant formulations. Environ Toxicol Chem 34(8):1881–1890
Latiff KA, Bakar NKA, Isa NM (2010) Preliminary study of difenoconazole residues in rice paddy watersheds. Malaysian J Sci 29:73–79
Lehner PN (1996) Handbook of ethological methods. Cambridge University Press, United Kingdom, p 672
Li S, Tan Y (2011) Hormetic response of cholinesterase from Daphnia magna in chronic exposure to triazophos and chlorpyrifos. J Environ Sci 23(5):852–859
Liu JF, Wu HM, Ma XS, Ding W (2011) Degradation of two diferente formulations of abamectin in paddy soil and paddy water. Acta Agric Zhejiangensis 023:4
Maltby L, Blake N, Brock TCM, Van den Brink PJ (2005) Insecticide speciessensitivity distributions: importance of test species selection and relevance toaquatic ecosystems. Environ Toxicol Chem 24:379–388
Mansano AS, Moreira RA, Dornfeld HC, Diniz LGR, Vieira EM, Daam MA, Rocha O, Seleghim MHR (2016) Acute and chronic toxicity of diuron andcarbofuran to the neotropical cladoceran Ceriodaphnia silvestrii. Environ Sci Pollut 25(14):13335–13346
Montagner CC, Vidal C, Acayaba RD, Jardim WF, Jardim ICSF, Umbuzeiro GA (2014) Trace analysis of pesticides and an assessment of their occurrencein surface and drinking waters from the State of São Paulo (Brazil). Anal Methods 6:6668–6677
Moore MN, Depledge MH, Readman JW, Paul Leonard DR (2004) An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res Fundam Mol Mech Mutagen 552:247–268
Moreira RA, Mansano AS, Rocha O (2015) The toxicity of carbofuran to the freshwater rotifer, Philodina roseola. Ecotoxicology 24(3):604–615
Moreira RA, Daam MA, Vieira BH, Sanches ALM, Reghini MV, Mansano AS, Freitas EC, Espindola ELG, Rocha O (2017) Toxicity of abamectin and difenoconazole mixtures to a Neotropical cladoceran after simulated run-off and spray drift exposure. Aquat Toxicol 185:58–66
Morgan AJ, Sturzenbaum SR, Kille P (1999) A short overview of molecular biomarker strategies with particular regard to recent developments in earthworms. Pedobiologia 43:574–584
Novais SC, Amorim MJ (2013) Changes in cellular energy allocation in Enchytraeus albidus when exposed to dimethoate, atrazine, and carbendazim. Environ Toxicol Chem 32:2800–2807
Novelli A, Vieira BH, Braun AS, Mendes LB, Daam MA, Espíndola ELG (2016) Impact of runoff water from an experimental agricultural field appliedwith Vertimec®18EC (abamectin) on the survival, growth and gill morphologyof zebrafish juveniles. Chemosphere 144:1408–1414
Novelli A, Vieira BH, Cordeiro D, Cappelini LTD, Vieira EM, Espindola ELG (2012) Lethal effects of abamectin on the aquatic organisms Daphnia similis, Chironomus xanthus and Danio rerio. Chemosphere 86:36–40
Nunes MET (2010) Assessment of pesticides effects on soil fauna through ecotoxicological tests with Eisenia andrei (Annelida, Oligochaeta) and natural soil fauna community. Doctoral thesis University of São Paulo, Brazil
Nunes MET, Espindola ELG (2012) Sensitivity of Eisenia andrei (Annelida, Oligochaeta) to a commercial formulation of abamectin in avoidance tests withartificial substrate and natural soil under tropical conditions. Ecotoxicology 21:1063–1071
Organisation for Economic Cooperation and Development (OECD) (2000) Daphnia sp., acute immobilisation test. Revised proposal for updating guideline 202. OECD, Paris (France)
Oakes KD, Van Der Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463
Organisation for Economic Cooperation and Development (OECD) (2012) Test No. 211: Daphnia magna Reproduction Test. OECD Publishing, Paris
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358
Palma P, Palma VL, Matos C, Fernandes RM, Bohn A, Soares AMVM, Barbosa IR (2009) Effects of atrazine and endosulfan sulphate on the ecdysteroid system of Daphnia magna. Chemosphere 74:676–681
Pavlaki MD, Pereira R, Loureiro S, Soares AMVM (2011) Effects of binary mixtures on the life traits of Daphnia magna. Ecotoxicol Environ Saf 74:99–110
Pilling ED, Bromley-Challenor KAC, Walker CH, Jepson PC (1995) Mechanismof synergism between the pyrethroid insecticide λ cyhalothrin and theimidazole fungicide prochloraz, in the honeybee (Apis mellifera L.). Pestic Biochem Physiol 51:1–11
PPDB - Pesticide Properties DataBase (2019) Freely accessible via https://sitem.herts.ac.uk/aeru/ppdb/en/ (Accessed 21 Nov 2019)
Printes LB, Callaghan A (2004) A comparative study on the relationship between acetylcholinesterase activity and acute toxicity in Daphnia magna exposed to anticholinesterase insecticides. Environ Toxicol Chem 23:1241–1247
Rhee JS, Kim BM, Jeong CB, Park H, Leung KMY, Lee YM, Lee JS (2013) Effect of pharmaceuticals exposure on acetylcholinesterase (AchE) activity and on the expression of AchE gene in the monogonont rotifer Brachionus koreanus. Comp Biochem Phys C 158:216–224
Ribeiro F, Nuno CG, Ferreira AF, Soares AMVM, Loureiro S (2011) Is ultraviolet radiation a synergistic stressor in combined exposures? The case study of Daphnia magna exposure to UV and carbendazim. Aquat Toxicol 102:114–122
Rodrigues ACM, Gravato C, Quintaneiro C, Barata C, Soares AMVM (2015) Sub-lethal toxicity of environmentally relevant concentrations of esfenvalerate to Chironomus riparius. Environ Pollut 207:273–279
Rodrigues ACM, Gravato C, Quintaneiro C, Bordalo MD, Golovko O, Žlábek V, Barata C, Amadeu MVM, Pestana JLT (2017) Exposure to chlorantraniliprole affects the energy metabolism of the caddisfly Sericostoma vittatum. Environ Toxicol Chem 36(6):1584–1591
Sanches ALM, Vieira BH, Reghini MV, Moreira RA, Freitas EC, Espíndola ELG, Daam MA (2017) Single and mixture toxicity of abamectin and difenoconazole to adult zebrafish (Danio rerio). Chemosphere 188:582–587
Santos MJG, Ferreira NGC, Soares AMVM, Loureiro S(2010) Toxic effects of molluscicidal baits to the terrestrial isopod Porcellionides pruinosus Brandt, 1833. J Soils Sediments 10:1335–1343
Saraiva AS, Sarmentoa RA, Rodrigues ACM, Campos D, Fedorovac G, Žlábekc V, Gravato C, Pestana JLT, Soares AMVM (2017) Assessment of thiamethoxam toxicity to Chironomus riparius. Ecotoxicol Environ Saf 137:240–246
Satapornvanit K, Baird DJ, Little DC, Milwain GK, Brink PJV, Beltman WHJ, Nogueira AJA, Daam MA, Domingues I, Kodithuwakku SS, Perera MWP, Yakupitiyage A, Sureshkumar SN, Taylor GJ (2004) Risks of pesticide use in aquatic ecosystems adjacent to mixed vegetable and monocrop fruit growing areas in Thailand. Aust J Ecotoxicol 10:85–95
Schäfer RB, Pettigrove V, Rose G, Allinson G, Wightwick A, Ohe PC, Shimeta J, Kühne R, Kefford BJ (2011) Effects of pesticides monitored with three sampling methods in 24 sites on macroinvertebrates and microorganisms. Environ Sci Technol 45:1665–1672
Shinn C, Delello-Schneider D, Mendes LB, Sanchez AL, Müller R, Espíndola ELG, Araújo CVM (2015) Immediate and mid-term effects of pyrimethanil toxicity on microalgae by simulating an episodic contamination. Chemosphere 120:407–413
Silva ARR, Cardoso DN, Cruz A, Lourenço J, Mendo S, Soares AMVM, Loureiro S (2015) Ecotoxicity and genotoxicity of a binary combination of triclosan and carbendazim to Daphnia magna. Ecotoxicol Environ Saf 115:279–290
Silva ARR, Santos CSA, Ferreira NGC, Morgado R, Cardoso DN, Cruz A, Mendo S, Soares AMVM, Loureiro S (2019) Multigenerational effects of carbendazim in Daphnia magna: From a subcellular to a population level. Enrion Toxicol Chem 38(2):412–422
Smolders R, De Boeck G, Blust R (2003) Changes in cellular energy budget as a measure of whole effluent toxicity in zebrafish (Danio rerio). Environ Toxicol Chem 22:890–899
Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15
Stein JR (1973) Standard Methods for the Examination of Water and Wastewater, 19th ed. American Public Health Association, Washington, p 1–1100
Subramoniam T (2000) Crustacean ecdysteriods in reproduction and embryogenesis. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 125:135–156
Syngenta (2019) Freely accessible via http://www.adapar.pr.gov.br/arquivos/File/defis/DFI/Bulas/Fungicidas/score230719.pdf (Accessed 20 Nov 2019)
Statsoft (2004) Statistica version 07. Freely accessible via www.statsoft.com (Accessed 16 Nov 2019)
Systat (2008) Systat Software, Incorporation SigmaPlot for Windows Version 11.0
Tagliari KC, Cecchini R, Rocha JAV, Vargas VMF (2004) Mutagenicity of sediment and biomarkers of oxidative stress in fish from aquatic environments under the influence of tanneries. Mutat Res-Gen Tox Environ 561:101–117
Teló GM, Marchesan E, Zanella R, Oliveira ML, Coelho LL, Martins ML (2015) Residues of fungicides and insecticides in rice field. Agron J 107:851–863
Tucca F, Díaz-Jaramillo M, Cruz G, Silva J, Bay-Schmith E, Chiang G, Barra R (2014) Toxic effects of antiparasitic pesticides used by the salmon industry in the marine amphipod Monocorophium insidiosum. Arch Environ Contam Toxicol 67(2):139–148
Tyne W, Little S, Spurgeon DJ, Svendsen C (2015) Hormesis depends upon the life-stage and duration of exposure: examples for a pesticide and a nanomaterial. Ecotox Environ Safe 120:117–123
United States Environmental Protection Agency (USEPA) (2002) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms, 5th edn. EPA-821-R-02–012, Washington
Vacchi FI, Von der Ohe PC, Albuquerque AF, Vendemiatti JAS, Azevedo CCJ, Honório JG, Silva BF, Zanoni MVB, Henry TB, Nogueira AJ, Umbuzeiro GA (2016) Occurrence and risk assessment of an azo dye and the case of Disperse Red 1. Chemosphere 156:95–100
Valavanidis A, Vlahogianni TH, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64(2):178–189
Vega MP, Pizarro RA (2000) Oxidative stress and defence mechanisms of the freshwater cladoceran Daphnia longispina exposed to UV radiation. J Photochem Photobiol B: Biol 54:121–125
Verslycke T, Roast SD, Widdows J, Jones MB, Janssen CR (2004) Cellular energy allocation and scope for growth in the estuarine mysid Neomysis integer (Crustacea: Mysidacea) following chlorpyrifos exposure: a method comparison. J Exp Mar Biol Ecol 306:1–16
Wang KS, Lu CY, Chang SH (2011) Evaluation of acute toxicity and teratogenic effects of plant growth regulators by Daphnia magna embryo assay. J Hazard Mater 190:520–528
Whittaker M, Wicks RJ, Judith J, Britten JJ (1982) Studies on the inhibition by propranolol of some human erythrocyte membrane enzymes and plasma cholinesterase. Clin Chim Acta 119(1-2):107–114
Wislocki PG, Grosso LS, Dybas RA (1989) Environmental aspects of abamectin use in crop protection. In: Campbell WC (Ed.) Ivermectin and Abamectin. Springer Verlag, New York, NY, USA, p 182–200
Zalizniak L, Nugegoda D (2006) Effect of sublethal concentrations of chlorpyrifos on three successive generations of Daphnia carinata. Ecotoxicol Environ Saf 64:207–214
Zhang Z, Wang D, Zhang C, Wu C, Liu X (2011) Difenoconazole residues in rice and paddy system. Chinese J Rice Sci 25:339–342
Acknowledgements
We thank CAPES (Process number: PDSE 88881.135987/2016-01). The National Council for Scientific and Technological Development (Process number: CNPq 201788/2014-4). This work also was supported by the Brazilian government through the Special Visiting Researcher program (MEC/MCTI/CAPES/CNPq/FAPs reference 402392/2013-2). Financial support was also provided to CESAM (UID/AMB/50017/2013) and CENSE (UID/AMB/04085/ 2013), by FCT/MEC through national funds, and the co-funding by the FEDER (POCI-01-0145-FEDER-00763), within the PT2020 Partnership Agreement and Compete 2020), through a postdoc grant for Michiel Adriaan Daam (SFRH/BPD/109199/2015). RAM has a pos doctoral fellowship from FAPESP (grant no. 2017/24126-4).
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Moreira, R.A., de Araujo, G.S., Silva, A.R.R.G. et al. Effects of abamectin-based and difenoconazole-based formulations and their mixtures in Daphnia magna: a multiple endpoint approach. Ecotoxicology 29, 1486–1499 (2020). https://doi.org/10.1007/s10646-020-02218-z
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DOI: https://doi.org/10.1007/s10646-020-02218-z