Abstract
The biobed is a purification system, which reduces soil pollution for receiving pesticide residues from handling and washing machinery in agricultural areas. The aims of this study were (1) to assess ecotoxicity effects over time to soil fauna, posed by Lorsban® 480 BR (Chlorpyrifos) and Dithane® NT (Mancozeb) residues when disposed of in a biobed system compared with two subtropical soils, and (2) to assess ecotoxicity effects over time to soil fauna simulating an accidental spillage with Lorsban® 480 BR at the biobed. A semi-field experiment was conducted for 420 days in southern Brazil, testing continuous disposal of washing pulverization tanks in biobeds, Typic Haploperox or Typic Hapludults. In addition, different biobeds received a single dose (1 L) of Lorsban® 480 BR to simulate an accidental spillage. Chronic ecotoxicity tests were performed using Folsomia candida, Eisenia andrei, and Enchytraeus crypticus in different sampling times for both experiments. F. candida was the most sensitive species. The biobed system was able to eliminate effects from residues of both pesticides over time in all species, which did not happen in both natural soils. In accidental spillage simulation, even 420 days after contamination, F. candida did not show reproduction. The biobeds can be a feasible alternative for the disposal and treatment residues of pesticides, also for handling and washing pesticides activities. The system was efficient in promoting degradation and reducing ecotoxicity effects posed by Lorsban® 480 BR and Dithane® NT for soil fauna. It is a safe alternative to avoid soil contamination.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alves PRL, Cardoso EJBN, Martines AM, Sousa JP, Pasini A (2014) Seed dressing pesticides on springtails in two ecotoxicological laboratory tests. Ecotoxicol Environ Saf 105:65–71. https://doi.org/10.1016/j.ecoenv.2014.04.010.
Amorim MJB, Römbke J, Soares AMVM (2005) Avoidance behaviour of Enchytraeus albidus: effects of Benomyl, Carbendazim, phenmedipham and different soil types. Chemosphere 59:501–510. https://doi.org/10.1016/j.chemosphere.2005.01.057.
Anwar S, Liaquat F, Khan QM, Khalid ZM, Iqbal S(2009) Biodegradation of chlorpyrifos and its hydrolysis product 3,5,6-trichloro-2-pyridinol by Bacillus pumilus strain C2A1 J Hazard Mater 168:400–405. https://doi.org/10.1016/j.jhazmat.2009.02.059.
Bandow C, Coors A, Römbke J (2013) Enchytraeus bigeminus (Enchytraeidae, Oligochaeta) as a new candidate for ecotoxicological laboratory tests. Soil Org 85:103–112.
Baskaran S, Kookana RS, Naidu R (1999) Degradation of bifenthrin, chlorpyrifos and imidacloprid in soil and bedding materials at termiticidal application rates. Pestic Sci 55:1222–1228. https://doi.org/10.1002/(SICI)1096-9063(199912)55:123.0.CO;2-7
Brasil (1989) Lei n° 7.802, de 11 de Julho de 1989. Dispõe sobre a pesquisa, a experimentação, a produção, a embalagem e rotulagem, o transporte, o armazenamento, a comercialização, a propaganda comercial, a utilização, a importação, a exportação, o destino final dos resíduos e embalagens, o registro, a classificação, o controle, a inspeção e a fiscalização de agrotóxicos, seus componentes e afins, e dá outras providências. http://www.planalto.gov.br/ccivil_03/leis/l7802.htm. Accessed 1 Sep 2014.
Cardoso LS, Bergamaschi H, Bosco LC, Paula VA, Marodin GAB, Casamali B, Nachtigall GR (2012) Disponibilidades climáticas para macieira na região de Vacaria, RS. Ciênc Rural 42:1960–1967. https://doi.org/10.1590/S0103-84782012005000097.
Carniel LSC, Niemeyer JC, Oliveira Filho LCI, Alexandre D, Gebler L, Klauberg-Filho O (2019) The fungicide Mancozeb affects soil invertebrates in two subtropical Brazilian soils. Chemosphere 232:180–185. https://doi.org/10.1016/j.chemosphere.2019.05.179.
Carter A (2000) How pesticides get into water—and proposed reduction measures. Pestic Outlook 11:149–156. https://doi.org/10.1039/b006243j.
Castillo M, del P, Torstensson L, Stenström J (2008) Biobeds for environmental protection from pesticide use—a review. J Agric Food Chem 56:6206–6219. https://doi.org/10.1021/jf800844x.
Castro-Gutiérrez V, Masís-Mora M, Diez MC, Tortella GR, Rodríguez-Rodríguez CE (2017) Aging of biomixtures: effects on carbofuran removal and microbial community structure. Chemosphere 168:418–425. https://doi.org/10.1016/j.chemosphere.2016.10.065.
Chu X, Fang H, Pan X, Wang X, Shan M, Feng B, Yu Y (2008) Degradation of chlorpyrifos alone and in combination with chlorothalonil and their effects on soil microbial populations. J Environ Sci 20:464–469.
Coppola L, Pilar Castillo M, del, Vischetti C (2011) Degradation of isoproturon and bentazone in peat- and compost-based biomixtures. Pest Manag Sci 67:107–113. https://doi.org/10.1002/ps.2040.
Dias LA, Niemeyer JC, Gebler L, Itako AT (2020) Destination of pesticide residues on biobeds: State of the art and future perspectives in Latin America. Chemosphere 248. https://doi.org/10.1016/j.chemosphere.2020.126038
Diez MC (2010) Biological aspects involved in the degradation or organic pollutants. J Soil Sci Plant Nutr 10:244–267. https://doi.org/10.4067/S0718-95162010000100004.
EFSA—European Commission Health & Consumer Protection (2007) Opinion of the scientific panel on plant protection products and their residues on a request from the Commission related to the revision of Annexes II and III to Council Directive 91/414/EEC concerning the placing of plant protection products on the market. EFSA J 461:1–44.
Endlweber K, Schädler M, Scheu S (2006) Effects of foliar and soil insecticide applications on the collembolan community of an early set-aside arable field. Appl Soil Ecol 31:136–146. https://doi.org/10.1016/j.apsoil.2005.03.004.
Fait G, Nicelli M, Fragoulis G, Trevisan M, Capri E (2007) Reduction of point contamination sources of pesticide from a vineyard farm. Environ Sci Technol 41:3302–3308. https://doi.org/10.1021/es062706k.
Fang H, Yu Y, Chu X, Wang X, Yang X, Yu J (2009) Degradation of chlorpyrifos in laboratory soil and its impact on soil microbial functional diversity. J Environ Sci 21:380–386. https://doi.org/10.1016/S1001-0742(08)62280-9.
Fernández-Alberti S, Rubilar O, Tortella GR, Diez MC (2012) Chlorpyrifos degradation in a Biomix: effect of pre-incubation and water holding capacity. J Soil Sci Plant Nutr 12:785–799. https://doi.org/10.4067/S0718-95162012005000032.
Fogg P, Boxall ABA, Walker A, Jukes AA (2003) Pesticide degradation in a biobed composting substrate. Pest Manag Sci 59:527–537. https://doi.org/10.1002/ps.685.
Fountain MT, Brown VK, Gange AC, Symondson WOC, Murray PJ (2007) The effects of the insecticide chlorpyrifos on spider and Collembola communities. Pedobiologia 51:147–158. https://doi.org/10.1016/j.pedobi.2007.03.001.
Frouz J, Livečková M, Albrechtová J, Chroňáková A, Cajthaml T, Pižl V, Háněl L, Starý J, Baldrian P, Lhotáková Z, Šimáčková H, Cepáková Š (2013) Is the effect of trees on soil properties mediated by soil fauna? A case study from post-mining sites. Ecol Manag 309:87–95. https://doi.org/10.1016/j.foreco.2013.02.013.
García-Santos G, Keller-Forrer K (2011) Avoidance behaviour of Eisenia fetida to carbofuran, chlorpyrifos, mancozeb and metamidophos in natural soils from the highlands of Colombia. Chemosphere 84:651–656. https://doi.org/10.1016/j.chemosphere.2011.03.036.
Garcia MVB (2004) Effects of pesticides on soil fauna: development of ecotoxicological test methods for tropical regions. University of Bonn, Bonn.
Gebler L, Fialho FB (2011) Introduzindo critérios de risco em modelos de contaminação pontual para locais de carga de agrotóxicos. Pestic Rev Ecotoxicol Meio Ambient 21:85–94. https://doi.org/10.5380/pes.v21i0.25847.
Gebler L, Pizzutti IR, Cardoso CD, Klauberg Filho O, Miquelluti DJ, Santos RSS (2015) Biorreactors to organize the disposal of phytosanitary effluents of brazilian apple production. Chem Eng Trans 43:343–348.
Gonçalves MFM, Gomes SIL, Soares AMVM, Amorim MJB (2016) Enchytraeus crypticus (Oligochaeta) is able to regenerate—Considerations for a standard ecotoxicological species. Appl Soil Ecol 107:320–323. https://doi.org/10.1016/j.apsoil.2016.07.007.
IBAMA—Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (1996) Portaria normativa IBAMA no 84, de 15 de outubro de 1996. http://www.ibama.gov.br/phocadownload/portaria_ibama_84_96_alteracoes.pdf. Accessed 1 Sep 2014.
ISO—International Organization for Standardization (2012a) Soil quality—effects of pollutants on earthworms (Eienia fetida)—part 2: determination of effects on reproduction. ISO 11268-2. ISO, Geneva.
ISO—International Organization for Standardization (2012b) Soil quality—inhibition of reproduction of Collembola (Folsomia candida) by soil pollutants. ISO 11267. ISO, Geneva.
ISO—International Organization for Standardization (2014) Soil quality—effects of pollutants on Enchytraeidae (Enchytraeus sp.)—determination of effects on reproduction and survival. ISO 16387. ISO, Geneva.
Jegede OO, Owojori OJ, Römbke J (2017) Temperature influences the toxicity of deltamethrin, chlorpyrifos and dimethoate to the predatory mite Hypoaspis aculeifer (Acari) and the springtail Folsomia candida (Collembola). Ecotoxicol Environ Saf 140:214–221. https://doi.org/10.1016/j.ecoenv.2017.02.046.
Jordaan MS, Reinecke SA, Reinecke AJ (2012) Acute and sublethal effects of sequential exposure to the pesticide azinphos-methyl on juvenile earthworms (Eisenia andrei). Ecotoxicology 21:649–661. https://doi.org/10.1007/s10646-011-0821-z.
Kamoun IJ, Jegede OO, Owojori OJ, Bouzid J, Gargouri R, Römbke J (2018) Effects of deltamethrin, dimethoate, and chlorpyrifos on survival and reproduction of the collembolan Folsomia candida and the predatory mite Hypoaspis aculeifer in two African and two European soils. Integr Environ Assess Manag 14:92–104. https://doi.org/10.1002/ieam.1966.
Karanasios EC, Tsiropoulos NG, Karpouzas DG (2013) Quantitative and qualitative differences in the metabolism of pesticides in biobed substrates and soil. Chemosphere 93:20–28. https://doi.org/10.1016/j.chemosphere.2013.04.049.
Karas PA, Makri S, Papadopoulou ES, Ehaliotis C, Menkissoglu-Spiroudi U, Karpouzas DG (2016) The potential of organic substrates based on mushroom substrate and straw to dissipate fungicides contained in effluents from the fruit-packaging industry—is there a role for Pleurotus ostreatus? Ecotoxicol Environ Saf 124:447–454. https://doi.org/10.1016/j.ecoenv.2015.11.022.
Klein M (2015) ESCAPE—estimation of soil-concentrations after pesticide applications version 2.0. Fraunhofer-Institut Molekularbiologie und Angewandte Ökologie. Schmallenberg, Germany.
Kralj MB, Franko M, Trebše P (2007) Photodegradation of organophosphorus insecticides—investigations of products and their toxicity using gas chromatography–mass spectrometry and AChE-thermal lens spectrometric bioassay. Chemosphere 67:99–107. https://doi.org/10.1016/j.chemosphere.2006.09.039.
Kramer MG, Lajtha K, Thomas G, Sollins P (2009) Contamination effects on soil density fractions from high N or C content sodium polytungstate. Biogeochemistry 92:177–181. https://doi.org/10.1007/s10533-008-9268-6.
Kuperman RG, Checkai RT, Simini M, Phillips CT (2004) Manganese toxicity in soil for Eisenia fetida, Enchytraeus crypticus (Oligochaeta), and Folsomia candida (Collembola). Ecotoxicol Environ Saf 57:48–53. https://doi.org/10.1016/j.ecoenv.2003.08.010.
Leitão S, Cerejeira MJ, Van den Brink PJ, Sousa JP (2014) Effects of azoxystrobin, chlorothalonil, and ethoprophos on the reproduction of three terrestrial invertebrates using a natural Mediterranean soil. Appl Soil Ecol 76:124–131. https://doi.org/10.1016/j.apsoil.2013.12.013.
Luan Y, Mallatt JM, Xie R, Yang Y, Yin W (2005) The phylogenetic positions of three basal-hexapod groups (Protura, Diplura, and Collembola) based on ribosomal RNA gene sequences. Mol Biol Evol 22:1579–1592. https://doi.org/10.1093/molbev/msi148.
Marichal R, Praxedes C, Decaëns T, Grimaldi M, Oszwald J, Brown GG, Desjardins T, Silva ML, Feijoo Martinez., Oliveira MND, Velasquez E, Lavelle P (2017) Earthworm functional traits, landscape degradation and ecosystem services in the Brazilian Amazon deforestation arc. Eur J Soil Biol 83:43–51. https://doi.org/10.1016/j.ejsobi.2017.09.003.
Matos AT, Fontes MPF, da Costa LM, Martinez MA (2001) Mobility of heavy metals as related to soil chemical and mineralogical characteristics of Brazilian soils. Environ Pollut 111:429–435. https://doi.org/10.1016/S0269-7491(00)00088-9.
Meier U (ed.) (2001) Growth stages of mono- and dicotyledonous plants. BBCH Monograph. Blackwell Wissenshafts-Verlag, Berlin, Germany, p 158.
Monaci E, Coppola L, Casucci C, Perucci P, Vischetti C (2009) Retention capacity of an organic bio-mixture against different mixtures of fungicides used in vineyards. J Environ Sci Health Part B 44:724–729. https://doi.org/10.1080/03601230903163889.
Morgado RG, Gomes PAD, Ferreira NGC, Cardoso DN, Santos MJG, Soares AMVM, Loureiro S (2016) Toxicity interaction between chlorpyrifos, mancozeb and soil moisture to the terrestrial isopod Porcellionides pruinosus. Chemosphere 144:1845–1853. https://doi.org/10.1016/j.chemosphere.2015.10.034.
Mukherjee S, Weihermüller L, Tappe W, Hofmann D, Köppchen S, Laabs V, Vereecken H, Burauel P (2016) Sorption–desorption behaviour of bentazone, boscalid and pyrimethanil in biochar and digestate based soil mixtures for biopurification systems. Sci Total Environ 559:63–73. https://doi.org/10.1016/j.scitotenv.2016.03.145.
Natal-da-Luz T, Moreira-Santos M, Ruepert C, Castillo LE, Ribeiro R, Sousa JP (2012) Ecotoxicological characterization of a tropical soil after diazinon spraying. Ecotoxicology 21:2163–2176. https://doi.org/10.1007/s10646-012-0970-8.
Novais SC, Soares AMVM, Amorim MJB (2010) Can avoidance in Enchytraeus albidus be used as a screening parameter for pesticides testing? Chemosphere 79:233–237. https://doi.org/10.1016/j.chemosphere.2010.01.011.
OECD—Organization for Economic Co-Operation and Development (2016) Test No. 222: earthworm reproduction test (Eisenia fetida/Eisenia andrei). OECD Guidelines for the Testing of Chemicals, Section 2, OECD Publishing, Paris, https://doi.org/10.1787/9789264264496-en.
Owojori OJ, Waszak K, Roembke J (2014) Avoidance and reproduction tests with the predatory mite Hypoaspis aculeifer: Effects of different chemical substances. Environ Toxicol Chem 33:230–237. https://doi.org/10.1002/etc.2421.
Pelosi C, Barot S, Capowiez Y, Hedde M, Vandenbulcke F (2014) Pesticides and earthworms. A review. Agron Sustain Dev 34:199–228. https://doi.org/10.1007/s13593-013-0151-z.
Pelosi C, Römbke J (2016) Are Enchytraeidae (Oligochaeta, Annelida) good indicators of agricultural management practices? Soil Biol Biochem 100:255–263. https://doi.org/10.1016/j.soilbio.2016.06.030.
Pérez-Parada A, Goyenola G, Teixeira de Mello F, Heinzen H (2018) Recent advances and open questions around pesticide dynamics and effects on freshwater fishes. Curr Opin Environ Sci Health 4:38–44. https://doi.org/10.1016/J.COESH.2018.08.004.
Reichenberger S, Bach M, Skitschak A, Frede H-G (2007) Mitigation strategies to reduce pesticide inputs into ground- and surface water and their effectiveness; a review. Sci Total Environ 384:1–35. https://doi.org/10.1016/j.scitotenv.2007.04.046.
Roffignac L, Cattan P, Mailloux J, Herzog D, Le Bellec F (2008) Efficiency of a bagasse substrate in a biological bed system for the degradation of glyphosate, malathion and lambda-cyhalothrin under tropical climate conditions. Pest Manag Sci 64:1303–1313. https://doi.org/10.1002/ps.1633.
Rufato L, Fachinello JC, Rossi A, Loeck AE (2006) Pátio de preparação de caldas de pulverização e eliminação de resíduos de agrotóxicos. UFPel;UDESC. http://www.ufpel.edu.br/pif/wp-content/uploads/2011/01/Local-de-preparo-de-agrot%C3%B3xicos.pdf.
Ruppert EE, Fox RS, Barnes RD (2005) Zoologia dos invertebrados, 7th edn. Editora Roca, São Paulo.
Santos MJG, Ferreira MFL, Cachada A, Duarte AC, Sousa JP (2012) Pesticide application to agricultural fields: effects on the reproduction and avoidance behaviour of Folsomia candida and Eisenia andrei. Ecotoxicology 21:2113–2122. https://doi.org/10.1007/s10646-012-0963-7.
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089.
Silva PMCS, Pathiratne A, van Gestel CAM (2009) Influence of temperature and soil type on the toxicity of three pesticides to Eisenia andrei. Chemosphere 76:1410–1415. https://doi.org/10.1016/j.chemosphere.2009.06.006.
Singh BK, Walker A, Morgan JAW, Wright DJ (2003) Effects of soil pH on the biodegradation of chlorpyrifos and isolation of a chlorpyrifos-degrading bacterium. Appl Environ Microbiol 69:5198–5206. https://doi.org/10.1128/AEM.69.9.5198-5206.2003.
Spadotto CA, Gomes MA, Luchini LC, Andreá M (2004) Monitoramento do risco ambiental de agrotóxicos: princípios e recomendações. Jaguariúna, Embrapa Meio Ambiente, p 29.
Spliid NH, Helweg A, Heinrichson K (2006) Leaching and degradation of 21 pesticides in a full-scale model biobed. Chemosphere 65:2223–2232. https://doi.org/10.1016/j.chemosphere.2006.05.049.
Soil Survey Staff (2014) Keys to soil taxonomy, 12th edn. U.S. Department of Agriculture, Natural Resources Conservation Service, Washington, DC.
StatSoft Inc. (2004) STATISTICA (data analysis software system) Version 7. www.statsoft.com.
Tedesco MJ, Gianello C, Bissani CA, Volkweiss SJ (1995) Análises de solo, plantas e outros materiais. Universidade Federal do Rio Grande do Sul, Porto Alegre.
Tortella GR, Mella-Herrera RA, Sousa DZ, Rubilar O, Briceño G, Parra L, Diez MC (2013) Carbendazim dissipation in the biomixture of on-farm biopurification systems and its effect on microbial communities. Chemosphere 93:1084–1093. https://doi.org/10.1016/j.chemosphere.2013.05.084.
Tortella GR, Rubilar O, Castillo MP, Cea M, Mella-Herrera R, Diez MC (2012) Chlorpyrifos degradation in a biomixture of biobed at different maturity stages. Chemosphere 88:224–228. https://doi.org/10.1016/j.chemosphere.2012.02.072.
UK Government (2014) Waste exemption: T32 treatment of waste in a biobed or biofilter. https://www.gov.uk/guidance/waste-exemption-t32-treatment-of-waste-in-a-biobed-or-biofilter. Accessed 7 Feb 2019.
Uddin MK (2017) A review on the adsorption of heavy metals by clay minerals, with special focus on the past decade. Chem Eng J 308:438–462. https://doi.org/10.1016/j.cej.2016.09.029.
Urrutia C, Rubilar O, Tortella G, Castillo JM, Romero E, Azcón R, Castillo MP, Diez MC (2015) Influence of the rhizosphere in a biopurification system on the dissipation of a pesticide mixture. J Soil Sci Plant Nutr 15:914–927. https://doi.org/10.4067/S0718-95162015005000063.
Vischetti C, Monaci E, Cardinali A, Casucci C, Perucci P (2008) The effect of initial concentration, co-application and repeated applications on pesticide degradation in a biobed mixture. Chemosphere 72:1739–1743. https://doi.org/10.1016/j.chemosphere.2008.04.065.
Zhang L, Van Gestel CAM (2019) Effect of ageing and chemical form on the bioavailability and toxicity of Pb to the survival and reproduction of the soil invertebrate Enchytraeus crypticus. Sci Total Environ 664:975–983. https://doi.org/10.1016/j.scitotenv.2019.02.054.
Zhang X, Luo Y, Goh KS (2018) Modeling spray drift and runoff-related inputs of pesticides to receiving water. Environ Pollut 234:48–58. https://doi.org/10.1016/j.envpol.2017.11.032.
Zortéa T, Reis TR, Serafini S, Sousa JP, Silva AS, Baretta D (2018) Ecotoxicological effect of fipronil and its metabolites on Folsomia candida in tropical soils. Environ Toxicol Pharmacol 62:203–209. https://doi.org/10.1016/j.etap.2018.07.011.
Acknowledgements
This study was funded by the National Council for Scientific and Technological Development (CNPq). LSCC thanks the Coordination for the Improvement of Higher Education Personnel (CAPES) for an M.Sc. grant. LCIOF holds a CNPq Scholarship—Brazil (155778/2018-8).
Author information
Authors and Affiliations
Corresponding author
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.
Supplementary information
Rights and permissions
About this article
Cite this article
Carniel, L.S.C., Niemeyer, J.C., de Oliveira Filho, L.C.I. et al. Are there any risks of the disposal of pesticide effluents in soils? Biobed system meets ecotoxicology ensuring safety to soil fauna. Ecotoxicology 29, 1409–1421 (2020). https://doi.org/10.1007/s10646-020-02260-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-020-02260-x