Skip to main content

Advertisement

Log in

Effects of abamectin-based and difenoconazole-based formulations and their mixtures in Daphnia magna: a multiple endpoint approach

  • Published:
Ecotoxicology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Meth Enzyme 105:121–126

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Bird RP, Draper HH (1984) Comparative studies on different methods of malonaldehyde determination. Methods Enzymol 105:299–305

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Calabrese EJ, Baldwin LA (2002) Defining hormesis. Hum Exp Toxicol 21(2):91–97

    CAS  Google Scholar 

  • Calabrese EJ, Baldwin LA (2003) Inorganics and hormesis. Crit Rev Toxicol 33:215–304

    CAS  Google Scholar 

  • Campbell WC (1989) Ivermectin and Abamectin. Springer Verlag, New York, NY

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Coors A, Frische T (2011) Predicting the aquatic toxicity of commercial pesticides mixtures. Environ Sci Europe 23/22:1–18

    Google Scholar 

  • Cox C, Surgan M (2006) Unidentified inert ingredients in pesticides: implicationsfor human and environmental health. Environ Health Perspect 114:1803–1806

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Deneer JW (2000) Toxicity of mixtures of pesticides in aquatic systems. Pest Manag Sci 56:516–520

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Forbes VE (2000) Is hormesis an evolutionary expectation? Funct Ecol 14:12–24

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Goulden CE, Henry L, Berrigan D (1987) Egg size, postembryonic yolk, and survival ability. Oecologia 72(1):28–31

    CAS  Google Scholar 

  • Guilhermino L, Lopes MC, Carvalho AP, Soares AM (1996) Acetylcholinesterase activity in juveniles of Daphnia magna Straus. Bull Environ Contam Toxicol 57:979–985

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotox Environ Safe 54:366–374

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Jiang H, Zhang XJ (2008) Acetylcholinesterase and apoptosis. A novel perspective for an old enzyme. FEBS J 275:612–617

    CAS  Google Scholar 

  • Johnson RM, Dahlgren L, Siegfried BD, Ellis MD (2013) Acaricide, fungicideand drug interactions in honey bees (Apis mellifera). PLoS ONE 8:e54092

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Latiff KA, Bakar NKA, Isa NM (2010) Preliminary study of difenoconazole residues in rice paddy watersheds. Malaysian J Sci 29:73–79

    CAS  Google Scholar 

  • Lehner PN (1996) Handbook of ethological methods. Cambridge University Press, United Kingdom, p 672

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Moreira RA, Mansano AS, Rocha O (2015) The toxicity of carbofuran to the freshwater rotifer, Philodina roseola. Ecotoxicology 24(3):604–615

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Organisation for Economic Cooperation and Development (OECD) (2000) Daphnia sp., acute immobilisation test. Revised proposal for updating guideline 202. OECD, Paris (France)

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Organisation for Economic Cooperation and Development (OECD) (2012) Test No. 211: Daphnia magna Reproduction Test. OECD Publishing, Paris

    Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Stein JR (1973) Standard Methods for the Examination of Water and Wastewater, 19th ed. American Public Health Association, Washington, p 1–1100

    Google Scholar 

  • Subramoniam T (2000) Crustacean ecdysteriods in reproduction and embryogenesis. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 125:135–156

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Zalizniak L, Nugegoda D (2006) Effect of sublethal concentrations of chlorpyrifos on three successive generations of Daphnia carinata. Ecotoxicol Environ Saf 64:207–214

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raquel Aparecida Moreira.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-020-02218-z

Keywords

Navigation