Abstract
In this study, we investigate the toxicity of commercial formulations based on glyphosate, 2,4-D, imidacloprid, and iprodione, in isolation and mixed, on Allium cepa. The mixtures consisted of combinations in the lowest (M1), intermediate (M2), and highest concentrations (M3) of each pesticide. We measured physiological (germination rate, germination speed, and radicular length) and cyto-genotoxic (mitotic index and frequency of aberrant cells) parameters. In addition, we analyzed the cell cycle progression and cell death induction by flow cytometry. When applied in isolation, the pesticides changed the parameters evaluated. M1 and M2 inhibited root length and increased the frequency of aberrant cells. Their genotoxic effect was equivalent to that of pesticides applied in isolation. Furthermore, M1 and M2 caused cell death and M2 changed the cell cycle progression. M3 had the greatest deleterious effect on A. cepa. This mixture inhibited root length and promoted an additive or synergistic effect on the mitotic index. In addition, M3 changed all parameters analyzed by flow cytometry. This research clearly demonstrates that the pesticides tested, and their mixtures, may pose a risk to non-target organisms.
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The data that support the funding of this study are available from the corresponding author, upon reasonable request.
References
Albuquerque AF, Ribeiro JS, Kummrow F, Nogueira AJA, Montagner CC, Umbuzeiro GA (2016) Pesticides in Brazilian freshwaters: a critical review. Environ Sci J Integr Environ Res: Process Impacts 18:779–787. https://doi.org/10.1039/c6em00268d
Alves TA, Pinheiro PF, Praça-Fontes MM, Andrade-Vieira LF, Lourenço MP, Lage MR, Alves TA, Cruz FA, Carneiro JWM, Ferreira A, Soares TCB (2021a) Bioactivity and molecular properties of phenoxyacetic acids derived from eugenol and guaiacol compared to the herbicide 2,4-D. An Acad Bras Cienc 93:e20191368. https://doi.org/10.1590/0001-3765202120191368
Alves TA, Roberto CEO, Pinheiro PF, Alves TA, Henrique MKC, Ferreira A, Clarindo WR, Praça-Fontes MM (2021b) Searching an auxinic herbicide to use as positive control in toxicity assays. An Acad Bras Cienc 93:e20181262. https://doi.org/10.1590/0001-3765202120181262
Andrade-Vieira LF, Campos JMS, Davide LC (2012) Effects of spent pot liner on mitotic activity and nuclear DNA content in meristematic cells of Allium cepa. J Environ Manag 107:140–146. https://doi.org/10.1016/j.jenvman.2012.04.008
Aragão FB, Queiroz VT, Ferreira A, Costa AV, Pinheiro PF, Carrijo TT, Vieira LFA (2017) Phytotoxicity and cytotoxicity of Lepidaploa rufogrisea (Asteraceae) extracts in the plant model Lactuca sativa (Asteraceae). Rev Biol Trop 65:435–443. https://doi.org/10.15517/rbt.v65i2.25696
Aragão FB, Bernardes PM, Ferreira A, Ferreira MFS, Andrade-Vieira LF (2019) Cyto(geno)toxicity of commercial fungicides based on the active compounds tebuconazole, difenoconazole, procymidone, and iprodione in Lactuca sativa L. meristematic cells. Water Air Soil Pollut 230:25. https://doi.org/10.1007/s11270-019-4080-6
Aranha A, Rocha L (2019) “Coquetel” com 27 agrotóxicos foi achado na água de 1 em cada 4 municípios. Agência Pública/ Repórter Brasil. Avaliable in https://portrasdoalimento.info/2019/04/15/coquetel-com-27-agrotoxicos-foi-achado-na-agua-de-1-em-cada-4-municipios/. Accessed August 2022
Araújo IMM, Oliveira AGRC (2017) Agronegócio e agrotóxicos: impactos à saúde dos trabalhadores agrícolas no Nordeste brasileiro. Trab Educ Saúde 15:117–129. https://doi.org/10.1590/1981-7746-sol00043
Barbosa AMC, Solano MLM, Umbuzeiro GA (2015) Pesticides in drinking water — the Brazilian monitoring program. Front Public Health 3:246. https://doi.org/10.3389/fpubh.2015.00246
Battaglin WA, Meyer MT, Kuivila KM, Dietze JE (2014) Glyphosate and its degradation product AMPA occur frequently and widely in U.S. soils, surface water, groundwater, and precipitation. J Am Water Resour Assoc 50:275–290. https://doi.org/10.1111/jawr.12159
Bernardes PM, Andrade-Vieira LF, Aragão FB, Ferreira A, Ferreira MFS (2019) Toxicological effects of commercial formulations of fungicides based on procymidone and iprodione in seedlings and root tip cells of Allium cepa. Environ Sci Pollut Res 26:21013–21021. https://doi.org/10.1007/s11356-019-04636-x
Bianchi J, Cabral-de-Mello DC, Marin-Morales MA (2015) Toxicogenetic effects of low concentrations of the pesticides imidacloprid and sulfentrazone individually and in combination in vitro tests with HepG2 cells and Salmonella typhimurium. Ecotoxicol Environ Safet 120:174–183. https://doi.org/10.1016/j.ecoenv.2015.05.040
Bianchi J, Fernandes TCC, Marin-Morales MA (2016) Induction of mitotic and chromosomal abnormalities on Allium cepa cells by pesticides imidacloprid and sulfentrazone and the mixture of them. Chemosphere 144:475–483. https://doi.org/10.1016/j.chemosphere.2015.09.021
Bickham JW, Sawin VL, Burton DW, McBee K (1992) Flow cytometric analysis of the effects of triethylenemelamine on somatic and testicular tissues of the rat. Cytom 13:368–373. https://doi.org/10.1002/cyto.990130406
Biradar DP, Rayburn AL (1995) Flow cytogenetic analysis of whole cell clastogenicity of herbicides found in groundwater. Arch Environ Contam Toxicol 28:13–17. https://doi.org/10.1007/BF00213963
Bortoluzzi EC, Rheinheimer DS, Gonçalves CS, Pellegrini JBR, Maroneze AM, Kurz MHS, Bacar NM, Zanella R (2007) Investigation of the occurrence of pesticides residues in rural wells and surface water following application to tobacco. Quím Nova 30:1872–1876. https://doi.org/10.1590/S0100-40422007000800014
Brovini EM, Deus BCT, Vilas-Boas JA, Quadra GR, Carvalho L, Mendonça RF, Pereira RO, Cardoso SJ (2021) Three-bestseller pesticides in Brazil: Freshwater concentrations and potential environmental risks. Sci Total Environ 771–144754. https://doi.org/10.1016/j.scitotenv.2020.144754
Bukowska (2006) Toxicity of 2,4-dichlorophenoxyacetic acid — molecular mechanisms. Polish J Environ Stud 15:365–374
Carneiro LS, Martínez LC, Gonçalves WG, Santana LM, Serrão JM (2020) The fungicide iprodione affects midgut cells of non-target honey bee Apis mellifera workers. Ecotoxicol Environ Saf 189:109991. https://doi.org/10.1016/j.ecoenv.2019.109991
Carvalho WF, Arcaute CR, Torres L, Silva DM, Soloneski S, Larramendy ML (2020) Genotoxicity of mixtures of glyphosate with 2,4-dichlorophenoxyacetic acid chemical forms towards Cnesterodon decemmaculatus (Pisces, Poeciliidae). Environ Sci Pollut Res 27:6515–6525. https://doi.org/10.1007/s11356-019-07379-x
Castro Berman M, Marino DJG, Quiroga MV, Zagarese H (2018) Occurrence and levels of glyphosate and AMPA in shallow lakes from the Pampean and Patagonian regions of Argentina. Chemosphere 200:513. https://doi.org/10.1016/j.chemosphere.2018.02.103
Chaufan G, Coalova I, Molina MCR (2014) Glyphosate commercial formulation causes cytotoxicity, oxidative ffects, and apoptosis on human cells: differences with its active ingredient. Int J Toxicol 33:29–38. https://doi.org/10.1177/1091581813517906
Chaufan G, Galvano C, Nieves M, Mudry MD, Molina MCR, Andrioli NB (2019) Oxidative response and micronucleus centromere assay in HEp-2 cells exposed to fungicide iprodione. Chem Res Toxicol 32:745–752. https://doi.org/10.1021/acs.chemrestox.8b00405
CONAMA – Conselho Nacional do Meio Ambiente. Resolução nº 357, de 17 de março de 2005. “Dispõe sobre a classificação dos corpos d’água e as diretrizes ambientais para sua classificação, bem como estabelece as condições e padrões de lançamento de efluentes e dá outras providências.” Diário Oficial da União, seção 1, Brasília, DF, n. 053, pp. 58–63, 18 mar. 2005 <http://www.siam.mg.gov.br/sla/download.pdf?idNorma=2747>. Accessed 10 June 2021
Demsia G, Vlastos D, Goumenou M, Matthopoulos DP (2007) Assessment of the genotoxicity of imidacloprid and metalaxyl in cultured human lymphocytes and rat bonemarrow. Mutat Res 634:32–39. https://doi.org/10.1016/j.mrgentox.2007.05.018
Directive (EU) (2020) 2020/2184 of the European Parliament and of the Council of 16 December 2020 on the quality of water intended for human consumption. Off J Eur Union 435:1–62. http://data.europa.eu/eli/dir/2020/2184/oj. Accessed July 2023
Felisbino K, Santos-Filho R, Piancini LDS, Cestari MM, Leme DM (2018) Mesotrione herbicide does not cause genotoxicity, but modulates the genotoxic effects of atrazine when assessed in mixture using a plant test system (Allium cepa). Pestic Biochem Physiol 150:83–88. https://doi.org/10.1016/j.pestbp.2018.07.009
Fenech M, Knasmueller S, Bolognesi C, Holland N, Bonassi S, Kirsch-Volders M (2020) Micronuclei as biomarkers of DNA damage, aneuploidy, inducers of chromosomal hypermutation and as sources of pro-inflammatory DNA in humans. Mutat Res/Rev Mutat Res 786:108342. https://doi.org/10.1016/j.mrrev.2020.108342
Finkler M, Rodrigues GZP, Kayser JM, Ziulkoski AL, Gehlen G (2022) Cytotoxic and genotoxic effects induced by associated commercial glyphosate and 2,4-D formulations using the Allium cepa bioassay. J Environ Sci Health Part B. https://doi.org/10.1080/03601234.2022.2034432
Fioresi VS, Vieira BCR, Campos JMS, Souza TS (2020) Cytogenotoxic activity of the pesticides imidacloprid and iprodione on Allium cepa root meristem. Environ Sci Pollut Res 27:28066–28076. https://doi.org/10.1007/s11356-020-09201-5
Fiskesjö G (1985) The Allium test as a standard in environmental monitoring. Hereditas 102:99–112. https://doi.org/10.1111/j.1601-5223.1985.tb00471.x
Flores-Céspedes F, Figueredo-Flores CI, Daza-Fernández I, Vidal-Peña F, Villafranca-Sánchez M, Fernández-Pérez M (2012) Preparation and characterization of imidacloprid lignin–polyethylene glycol matrices coated with ethylcellulose. J Agric Food Chem 60:1042–1051. https://doi.org/10.1021/jf2037483
Fossen M (2006) Environmental fate of imidacloprid. Environmental Monitoring. Department of Pesticide Regulation. Available Available in http://cues.cfans.umn.edu/old/pollinators/pdf-pesticides/2006CAImidclprdfate.pdf
Gadeva P, Dimitrov B (2008) Genotoxic effects of the pesticides Rubigan, Omite and Rovral in root-meristem cells of Crepis capillaris L. Mutat Res 652:191–197. https://doi.org/10.1016/j.mrgentox.2008.02.007
Galbraith DW, Harkins KR, Maddox JM, Ayres NM, Sharma DP, Firoozabady E (1983) Rapid flow cytometric analysis of the cell cycle in intact plant tissues. Science 220:1049–1051. https://doi.org/10.1126/science.220.4601.1049
George J, Shukla Y (2013) Emptying of intracellular calcium pool and oxidative stress imbalance are associated with the glyphosate-induced proliferation in human skin keratinocytes HaCaT cells. ISRN Dermatol 2013:25180. https://doi.org/10.1155/2013/825180
Ghosh M, Bhadra S, Adegoke A, Bandyopadhyay M, Mukherjee A (2015) MWCNT uptake in Allium cepa root cells induces cytotoxic and genotoxic responses and results in DNA hyper-methylation. Mutat Res/Fundam Mol Mech Mutagen 774:49–58. https://doi.org/10.1016/j.mrfmmm.2015.03.004
Ghosh M, Jana A, Sinha S, Jothiramajayam M, Nag A, Chakraborty A, Mukherjee A, Mukherjee A (2016) Effects of ZnO nanoparticles in plants: cytotoxicity, genotoxicity, deregulation of antioxidant defenses, and cell-cycle arrest. Mutat Res/Genet Toxicol Environ Mutagen 807:25–32. https://doi.org/10.1016/j.mrgentox.2016.07.006
Grabinska-Sota E, Wisniowska E, Kalka (2003) Toxicity of selected synthetic auxines—2,4-D and MCPA derivatives to broad-leaved and cereal plants. Crop Prot 22:355–360. https://doi.org/10.1016/S0261-2194(02)00178-3
Hanson B, Bond C, Buhl K, Stone D (2015) Pesticide half-life fact sheet. National Pesticide Information Center, Oregon State University Extension Services. Available in https://npic.orst.edu/factsheets/half-life.html. Accessed July 2023
IARC – International Agency for Research Cancer (2017) World Health Organization. Monographs on the identification of carcinogenesis hazards to humans. 112. https://publications.iarc.fr/549. Accessed 10 June 2022
IARC – International Agency for Research Cancer (2018) World Health Organization. Monographs on the identification of carcinogenesis hazards to humans. DDT, Lindane, and 2,4-D. 113. https://publications.iarc.fr/550. Accessed 10 June 2022
IBAMA – Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, Relatórios de Comercialização de Agrotóxicos – Boletim Anual de Produção, Importação, Exportação e Vendas de Agrotóxicos no Brasil. https://www.gov.br/ibama/pt-br/assuntos/quimicos-e-biologicos/agrotoxicos/relatorios-de-comercializacao-de-agrotoxicos#boletinsanuais. Accessed 12 November 2022
Iturburu FG, Simoniello MF, Medici S, Panzeri AM, Menone ML (2018) Imidacloprid causes DNA damage in fish: clastogenesis as a mechanism of genotoxicity. Bull Environ Contam Toxicol 100:760–764. https://doi.org/10.1007/s00128-018-2338-0
Karabay NU, Oguz MG (2005) Cytogenetic and genotoxic effects of the insecticides, imidacloprid and methamidophos. Genet Mol Res 4:653–662
Kier LD, Kirkland DJ (2013) Review of genotoxicity studies of glyphosate and glyphosate-based formulations. Crit Rev Toxicol 43:283–315. https://doi.org/10.3109/10408444.2013.770820
MAPA - Ministério da Agricultura, Pecuária e Abastecimento. Sistema de Agrotóxicos Fitossanitários. https://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 16 July 2022
Marc J, Bellé R, Morales J, Cormier P, Mulner-Lorillon O (2004) Formulated glyphosate activates the dna-response checkpoint of the cell cycle leading to the prevention of G2/M transition. Toxicol Sci 82:436–442. https://doi.org/10.1093/toxsci/kfh281
Marcato ACC, Souza CP, Fontanetti CS (2017) Herbicide 2,4-D: a review of toxicity on non-target organisms. Water Air Soil Pollut 228:1–12. https://doi.org/10.1007/s11270-017-3301-0
Mazzeo DEC, Fernandes TCC, Levy CE, Fontanetti CS, Marin-Morales MA (2015) Monitoring the natural attenuation of a sewage sludge toxicity using the Allium cepa test. Esological Indic 56:60–69. https://doi.org/10.1016/j.ecolind.2015.03.026
Mercado SAS, Caleño JDQ (2020) Cytotoxic evaluation of glyphosate, using Allium cepa L. as bioindicator. Sci Total Environ 700:134452. https://doi.org/10.1016/j.scitotenv.2019.134452
Mondal S, Kumar M, Haque S, Kundu D (2017) Phytotoxicity of glyphosate in the germination of Pisum sativum and its effect on germinated seedlings. Environ Health Toxicol 32:e2017011. https://doi.org/10.5620/eht.e2017011
Monteiro MS, Rodriguez E, Loureiro J, Mann RM, Soares AMVM, Santos C (2010) Flow cytometric assessment of Cd genotoxicity in three plants with different metal accumulation and detoxification capacities. Ecotoxicol Environ Saf 73:1231–1237. https://doi.org/10.1016/j.ecoenv.2010.06.020
Moreira NCS, Lima JEBF, Sakamoto-Hojo ET (2021) Citometria de fluxo – fundamentos, aplicações e análise do ciclo celular e apoptose. In: Salvadori DMF, Takahashi CS, Grisolia CK (eds) Da Toxicogenética à Toxicogenômica. Santos, R.A. 1 ed – Rio de Janeiro: Atheneu, p 388
MS - Ministério da Saúde. Portaria no. 2.914 de 12 de dezembro de (2011) Dispõe sobre os procedimentos de controle e de vigilância da qualidade da água para consumo humano e seu padrão de potabilidade. Diário Oficial da União, Brasília, 14 de dezembro de 2011. https://bvsms.saude.gov.br/bvs/saudelegis/gm/2011/prt2914_12_12_2011.html. Accessed 10 April 2020
NPCI - National Pesticide Information Center (2011) Oregon University State. 2,4-D Technical Fact Sheet. Available in http://npic.orst.edu/factsheets/archive/2,4-DTech.html. Accessed July 2023
Piotrowicz-Cieślak AI, Adomas B, Michalczyk DJ (2010) Different glyphosate phytotoxicity to seeds and seedlings of selected plant species. Pol J Environ Stud 19:123–129
Queiroz VT, Azevedo MM, Quadros IPS, Costa AV, Amaral AA, Amaral GM, Santos DA, Juvanhol RS, Telles LAA, Santos AR (2018) Environmental risk assessment for sustainable pesticide use in coffee production. J Contam Hydrol 219:18–27. https://doi.org/10.1016/j.jconhyd.2018.08.008
Rank J, Nielsen MH (1994) Evaluation of the Allium anaphase-telophase test in relation to genotoxicity screening of industrial wastewater. Mutat Res 312:17–24. https://doi.org/10.1016/0165-1161(94)90004-3
Rayburn AL, Wetzel JB (2002) Flow cytometric analyses of intraplant nuclear DNA content variation induced by sticky chromosomes. Cytometry 49:36–41. https://doi.org/10.1002/cyto.10135
Rodrigues LB, Costa GG, Thá EL, Silva LR, Oliveira R, Leme DM, Cestari MM, Grisolia CK, Valadares MC, Oliveira GAR (2019) Impact of the glyphosate-based commercial herbicide, its components and its metabolite AMPA on non-target aquatic organisms. Mutat Res 842:94–101. https://doi.org/10.1016/j.mrgentox.2019.05.002
Rodríguez YA, Christofoletti CA, Pedro J, Bueno OC, Fontanetti CS (2015) Allium cepa and Tradescantia pallida bioassays to evaluate effects of the insecticide imidacloprid. Chemosphere 120:438–442. https://doi.org/10.1016/j.chemosphere.2014.08.022
Samojeden CG, Pavan FA, Rutkoski CF, Folador A, Fré SP, Müller C, Hartmann PA, Hartmann M (2022) Toxicity and genotoxicity of imidacloprid in the tadpoles of Leptodactylus luctator and Physalaemus cuvieri (Anura: Leptodactylidae). Sci Rep 12:11926. https://doi.org/10.1038/s41598-022-16039-z
Sequinatto L, Reichert JM, Santos DR, Reinert DJ, Copetti ACC (2013) Occurrence of agrochemicals in surface waters of shallow soils and steep slopes cropped to tobacco. Quím Nova 36:768–772
Shuma JM, Quick WA, Raju MV, Hsiao AI (1995) Germination of seeds from plants of Avenafatua L. treated with glyphosate. Weed Res 35:249–255. https://doi.org/10.1111/j.1365-3180.1995.tb01787.x
Silva LCM, Moreira RA, Pinto TJS, Ogura AP, Yoshii MPC, Lopes LFP, Montagner CC, Goulart BV, Daam MA, Espíndola ELG (2020) Acute and chronic toxicity of 2,4-D and fipronil formulations (individually and in mixture) to the Neotropical cladoceran Ceriodaphnia silvestrii. Ecotoxicology 29:1462–1475. https://doi.org/10.1007/s10646-020-02275-4
Souza TS, Barone LSF, Lacerda D, Vergilio CS, Oliveira BCV, Almeida MG, Thompson F, Rezende C (2021) Cytogenotoxicity of the water and sediment of the Paraopeba River immediately after the iron ore mining dam disaster (Brumadinho, Minas Gerais, Brazil). Sci Total Environ 775:145193. https://doi.org/10.1016/j.scitotenv.2021.145193
Souza VV, Silva Souza T, Campos JMS, Oliveira LA, Ribeiro YM, Melo Hoyos DC, Xavier RMP, Charlie-Silva I, Lacerda SMSN (2023) Ecogenotoxicity of environmentally relevant atrazine concentrations: a threat to aquatic bioindicators. Pestic Biochem Physiol 189:105297. https://doi.org/10.1016/j.pestbp.2022.105297
Truta E, Vochita G, Rosu C, Zamfirache M-M, Olteanu Z (2011) Evaluation of roundup-induced toxicity on genetic material and on length growth of barley seedlings. Acta Biol Hung 62:290–301. https://doi.org/10.1556/ABiol.62.2011.3.8
Türkoğlu S (2012) Determination of genotoxic effects of chlorfenvinphos and fenbuconazole in Allium cepa root cells by mitotic activity, chromosome aberration, DNA content, and comet assay. Pestic Biochem Physiol 103:224–230. https://doi.org/10.1016/j.pestbp.2012.06.001
US Environmental Protection Agency (USEPA) (1996) Seed germination/root elongation toxicity test, OPPTS 850.4200, EPA 712/C-96/154. Ecological effects test guidelines. EPA 712-C-96-154. Washington, DC
US Environmental Protection Agency (EPA) (2007) Office of Prevention, Pesticides and Toxic Substances. Iprodione drinking water assessment, including proposed new use on pistachio (IR4) and label revisions affecting rates for strawberries, stone fruits, and grapes. DP Barcode: D285550. p 22. Available in https://ordspub.epa.gov/ords/pesticides/f?p=CHEMICALSEARCH:7::::1,3,31,7,12,25:P3_XCHEMICAL_ID:2597. Accessed July 2023
van der Meer FJ, Faber DJ, Aalders MCG, Poot AA, Vermes I, van Leeuwen TG (2010) Apoptosis- and necrosis-induced changes in light attenuation measured by optical coherence tomography. Lasers Med Sci 25:259–267. https://doi.org/10.1007/s10103-009-0723-y
Vieira C, Marcon C, Droste A (2022) Phytotoxic and cytogenotoxic assessment of glyphosate on Lactuca sativa L. Braz J Biol 84. https://doi.org/10.1590/1519-6984.257039
WHO - World Health Organization. Environmental Health Criteria 5 (1985) Guide to short-term tests for detecting mutagenic and carcinogenic chemicals. Geneva, p 208. Accessed in https://wedocs.unep.org/handle/20.500.11822/29495
Wlodkowic D, Telford W, Skommer J, Darzynkiewicz Z (2011) Apoptosis and beyond: cytometry in studies of programmed cell death. Methods Cell Biol 103:55–98. https://doi.org/10.1016/B978-0-12-385493-3.00004-8
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This work was supported by the Fundação de Amparo à Pesquisa do Espírito Santo — FAPES (No. 14/2019-PROCAP 2020). Luanna Alves Miranda has received from FAPES Master fellowship 096/2020.
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Conceptualization was performed by Tatiana da Silva Souza and Victor Ventura de Souza. Material preparation, data collection, and analysis were performed by Luanna Alves Miranda, Renata Alice Campos, and José Marcello Salabert de Campos. The first draft of the manuscript was written by Luanna Alves Miranda. Writing — review and editing: Tatiana da Silva Souza. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Supervision: Tatiana da Silva Souza.
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Miranda, L.A., de Souza, V.V., Campos, R.A. et al. Phytotoxicity and cytogenotoxicity of pesticide mixtures: analysis of the effects of environmentally relevant concentrations on the aquatic environment. Environ Sci Pollut Res 30, 112117–112131 (2023). https://doi.org/10.1007/s11356-023-30100-y
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DOI: https://doi.org/10.1007/s11356-023-30100-y