Abstract
To attend the increasing demand for food and energy, vast monocultures such as sugarcane, soy, and corn, often adopts routinely intensive application of pesticides and chemical fertilizers, disregarding their potential effects on non-target soil organisms, which are crucial for soil functioning. In this study, we present the assessment of toxic effects of the commercial herbicide DMA® 806 BR (active ingredient: 2,4-D) and of the insecticide Regent® 800 WG (active ingredient: fipronil) to the non-target terrestrial plant Raphanus sativus var. acanthioformis (dicotyledon) and to the collembolan species Folsomia candida, in combination with different soil moisture conditions in natural and artificial tropical soils. Plant growth and biomass were severely affected by the presence of DMA alone, with significant differences from the control treatment already detected at 0.13 mg/kg/dw. Upon low soil moisture (20%, 40%, 60% WHC), the toxicity of DMA to plants was diminished, exhibiting an antagonistic pattern of interaction between DMA and soil moisture. Soil composition had a significant influence on survival and reproduction of collembola especially at high soil moisture content. In the natural soil, 80% of the water holding capacity (WHC) induced 100% collembola mortality whereas, in the tropical artificial soil (TAS), this same moisture condition had a negligible effect on survival. Reproduction was mainly affected by fipronil under drought conditions (20% WHC) at both soil types, possibly correlated with increased concentration of fipronil in the soil pore water at such conditions. Results herein presented highlight the requisite of including abiotic fluctuations in hazard assessment of pesticides to preserve soil function provided by biota.
Highlights
-
Soil moisture contribute on determining 2,4-D toxicity to terrestrial plants.
-
Soil moisture contribute on determining fipronil toxicity to Folsomia candida.
-
High-moisture levels increased plant species sensitivity to the herbicide 2,4-D.
-
Soil properties influences collembola sensitivity to pesticide contamination.
-
Dry conditions (20% WHC) + fipronil (1/8 RD) decrease F. candida
-
reproduction in 70%.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of Data and Materials
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
ABNT AB, de NT (2012) ABNT NBR ISO 16387:2012. Qualidade do solo - Efeitos de poluentes em Enchytraeidae (Enchytraeus sp.) - Determinação de efeitos sobre reprodução e sobrevivência
ABNT AB, de NT (2018) ABNT NBR ISO 11267:2019. Qualidade do solo — Inibição da reprodução de Collembola (Folsomia candida) por poluentes do solo
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
Aubin S, Elbeuf L (2018) Regent ® 800 WG 1–10
Bandow C, Karau N, Römbke J (2014) Interactive effects of pyrimethanil, soil moisture and temperature on Folsomia candida and Sinella curviseta (Collembola). Appl Soil Ecol 81:22–29. https://doi.org/10.1016/j.apsoil.2014.04.010
Bonmatin JM, Giorio C, Girolami V, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Long E, Marzaro M, Mitchell EA, Noome DA, Simon-Delso N, Tapparo A (2015) Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut Res 22:35–67. https://doi.org/10.1007/s11356-014-3332-7
Boscolo CNP, Felício AA, Pereira TSB, Margarido TCS, Rossa-Feres D, Almeida EA, Freitas JS (2017) Comercial insecticide fipronil alters antioxidant enzymes response and accelerates the metamorphosis in Physalaemus nattereri (Anura: Leiuperidae) tadpoles. Eur J Zool Res. 5:1–7
Braúlio Hennig T, Ogliari Bandeira F, Dalpasquale AJ, Cardoso EJBN, Baretta D, Lopes Alves PR (2020) Toxicity of imidacloprid to collembolans in two tropical soils under different soil moisture. J Environ Qual 49:1491–1501. https://doi.org/10.1002/jeq2.20143
Cenkci S, Yildiz M, Ciĝerci IH, Bozdaĝ A, Terzi H, Terzi ESA (2010) Evaluation of 2,4-D and Dicamba genotoxicity in bean seedlings using comet and RAPD assays. Ecotoxicol Environ Saf 73:1558–1564. https://doi.org/10.1016/j.ecoenv.2010.07.033
Christofoletti CA, Pereira C, Ansoar Y (2017) O emprego de agrotóxicos na cultura de cana-de-açúcar. In: Fontanetti CS, Bueno OC (Eds.), Cana-de-Açúcar e Seus Impactos : Uma Visão Acadêmica. Canal6, Rio Claro, pp. 51–61
de Amarante OP, Brito NM, dos Santos TCR, Nunes GS, Ribeiro ML (2003) Determination of 2,4-dichlorophenoxyacetic acid and its major transformation product in soil samples by liquid chromatographic analysis. Talanta 60(1):115–121. https://doi.org/10.1016/S0039-9140(03)00113-9
de Menezes Oliveira VB, de Oliveira Bianchi M, Espíndola ELG (2018) Hazard assessment of the pesticides KRAFT 36 EC and SCORE in a tropical natural soil using an ecotoxicological test battery. Environ Toxicol Chem 37(11):2919–2924. https://doi.org/10.1002/etc.4056
Domene X, Chelinho S, Campana P, Natal-da-Luz T, Alcañiz JM, Andrés P, Römbke J, Sousa P (2011) Influence of soil properties on the performance of Folsomia candida: Implications for its use in soil ecotoxicology testing. Environ Toxicol Chem 30:1497–1505. https://doi.org/10.1002/etc.533
European Commission (2009) Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC
Ferreira ALG, Serra P, Soares AMVM, Loureiro S (2010) The influence of natural stressors on the toxicity of nickel to Daphnia magna. Environ Sci Pollut Res 17:1217–1229. https://doi.org/10.1007/s11356-010-0298-y
Gunasekara AS, Truong T, Goh KS, Spurlock F, Tjeerdema RS (2007) Environmental fate and toxicology of fipronil. J Pestic Sci. https://doi.org/10.1584/jpestics.R07-02
Gupta RC, Milatovic D (2014) Insecticides, In: Gupta R (Ed.), biomarkers in toxicology. Elsevier Inc., pp. 389–407. https://doi.org/10.1016/B978-0-12-404630-6.00023-3
Højer R, Bayley M, Damgaard CF, Holmstrup M (2001) Stress synergy between drought and a common environmental contaminant: Studies with the collembolan Folsomia candida. Glob Chang Biol 7:485–494. https://doi.org/10.1046/j.1365-2486.2001.00417.x
Holmstrup M, Maraldo K, Krogh PH (2007) Combined effect of copper and prolonged summer drought on soil Microarthropods in the field. Environ Pollut 146:525–533. https://doi.org/10.1016/j.envpol.2006.07.013
IBAMA (2017) OS 10 ingredientes ativos mais vendidos
IBM Corp (2020) IBM SPSS Statistics for Windows, Version 27.0. IBM Corp, Armonk, NY
Islam F, Wang J, Farooq MA, Khan MSS, Xu L, Zhu J, Zhao M, Muños S, Li QX, Zhou W (2018) Potential impact of the herbicide 2,4-dichlorophenoxyacetic acid on human and ecosystems. Environ Int. https://doi.org/10.1016/j.envint.2017.10.020
Jänsch S, Amorim MJ, Römbke J (2005) Identification of the ecological requirements of important terrestrial ecotoxicological test species. Environ Rev 13:51–83. https://doi.org/10.1139/a05-007
Jonker MJ, Svendsen C, Bedaux JJ, Bongers M, Kammenga JE (2005) Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratiodependent effects in mixture dose-response analysis. Environ Toxicol Chem 24(10):2701–2713. https://doi.org/10.1897/04-431r.1
Krab EJ, Van Schrojenstein Lantman IM, Cornelissen JHC, Berg MP (2013) How extreme is an extreme climatic event to a subarctic peatland springtail community? Soil Biol. Biochem 59:16–24. https://doi.org/10.1016/j.soilbio.2012.12.012
Kumar S (2010) Effect of 2,4-D and Isoproturon on chromosomal disturbances during mitotic division in root tip cells of Triticum aestivum L. Cytol Genet 44:79–87. https://doi.org/10.3103/S0095452710020027
Lazar T, Taiz L, Zeiger E (2003) Plant physiology. 3rd ed., in: Annals of Botany. Sinauer Associates, pp. 750–751. https://doi.org/10.1093/aob/mcg079
Lima MP, Soares AM, Loureiro S (2011) Combined effects of soil moisture and carbaryl to earthworms and plants: simulation of flood and drought scenarios. Environ Pollut 159(7):1844–1851. https://doi.org/10.1016/j.envpol.2011.03.029
Liu F, Stützel H (2004) Biomass partitioning, specific leaf area, and water use efficiency of vegetable amaranth (Amaranthus spp.) in response to drought stress. Sci Hortic (amsterdam) 102:15–27. https://doi.org/10.1016/j.scienta.2003.11.014
Luiz Lonardoni Foloni (2016) O herbicida 2,4-D. Uma visão geral, 1st edn. LabcomTotal. LabcomTotal, Ribeirão Preto
Marcato AC, Souza C, Fontanetti CP (2017) Herbicide 2,4-D: A Review of Toxicity on Non-Target Organisms. Water Air Soil Pollut. https://doi.org/10.1007/s11270-017-3301-0
Menezes-Oliveira VB, Scott-Fordsmand JJ, Soares AMVM, Amorim MJB (2014) Development of ecosystems to climate change and the interaction with pollution—Unpredictable changes in community structures. Appl Soil Ecol 75:24–32. https://doi.org/10.1016/j.apsoil.2013.10.004
Natal-Da-Luz T, Römbke J, Sousa JP (2008) Avoidance tests in site-specific risk assessment - Influence of soil properties on the avoidance response of Collembola and earthworms. Environ Toxicol Chem 27:1112–1117. https://doi.org/10.1897/07-386.1
Nogueira Cardoso EJB, Lopes Alves PR (2012) Soil ecotoxicology, in: ecotoxicology. IntechOpen https://doi.org/10.5772/28447
Pinto TJDS, Rocha GS, Moreira RA, Silva LCMD, Yoshii MPC, Goulart BV, Montagner CC, Daam MA, Espindola ELG (2021a) Multi-generational exposure to fipronil, 2,4-D, and their mixtures in Chironomus sancticaroli: Biochemical, individual, and population endpoints. Environ Pollut 283:117384. https://doi.org/10.1016/j.envpol.2021.117384
Pinto TJDS, Moreira RA, Silva LCMD, Yoshii MPC, Goulart BV, Fraga PD, Montagner CC, Daam MA, Espindola ELG (2021b) Impact of 2,4-D and fipronil on the tropical midge Chironomus sancticaroli (Diptera: Chironomidae). Ecotoxicol Environ Saf 209:111778
Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser DP, Krupke C, Liess M, Mcfield M, Morrissey CA, Noome DA, Settele J, Simon-Delso N, Stark JD, Van Der Sluijs JP, Van Dyck H, Wiemers M (2014) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68–102. https://doi.org/10.1007/s11356-014-3471-x
Rodríguez-Cruz M, Sánchez-Martín M, Andrades M, Sánchez-Camazano M (2006) Comparison of pesticide sorption by physicochemically modified soils with natural soils as a function of soil properties and pesticide hydrophobicity. Soil Sediment Contam 15:401–415. https://doi.org/10.1080/15320380600751769
Römbke J, García M (2000) Assessment of Ecotoxicological effects of pesticides on the soil fauna and soil processes under tropical conditions. Proc Ger. 1999:543–549
Schneider C, Rasband W, Eliceiri K (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
Silva LC, da Moreira RA, Rocha O (2012). A Toxicidade Aguda Do Agrotóxico Fipronil Para O Cladócero Bosmina Freyi De Melo and Hebert, 1994. Periódico Eletrônico Fórum Ambient. da Alta Paul. 8, 384–394. https://doi.org/10.17271/19800827822012267
Singh A, Srivastava A, Srivastava PC (2016) Sorption-desorption of fipronil in some soils, as influenced by ionic strength, pH and temperature. Pest Manag Sci 72:1491–1499. https://doi.org/10.1002/ps.4173
Skovlund G, Damgaard C, Bayley M, Holmstrup M (2006) Does lipophilicity of toxic compounds determine effects on drought tolerance of the soil collembolan Folsomia candida? Environ Pollut 144:808–815. https://doi.org/10.1016/j.envpol.2006.02.009
Song Y (2014) Insight into the mode of action of 2,4-dichlorophenoxyacetic acid (2,4-D) as an herbicide. J Integr Plant Biol 56(2):106–113. https://doi.org/10.1111/jipb.12131
Spark KM, Swift RS (2002) Effect of soil composition and dissolved organic matter on pesticide sorption. Sci Total Environ 298:147–161. https://doi.org/10.1016/S0048-9697(02)00213-9
Trenberth KE (2011) Changes in precipitation with climate change. Clim Res 47:123–138. https://doi.org/10.3354/cr00953
Triques MC, Oliveira D, Goulart BV, Montagner CC, Espíndola ELG, de Menezes-Oliveira VB (2021) Assessing single effects of sugarcane pesticides fipronil and 2,4-D on plants and soil organisms. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2020.111622
Van Gestel CAM, Mol S (2003) The influence of soil characteristics on cadmium toxicity for Folsomia candida (Collembola: Isotomidae). Pedobiologia (jena) 47:387–395. https://doi.org/10.1007/s00128-016-1792-9
Van Gestel CAM, Van Diepen AMF (1997) The influence of soil moisture content on the bioavailability and toxicity of cadmium for Folsomia candida Willem (Collembola: Isotomidae). Ecotoxicol Environ Saf 36:123–132. https://doi.org/10.1006/eesa.1996.1493
Waalewijn-Kool PL, Rupp S, Lofts S, Svendsen C, van Gestel CAM (2014) Effect of soil organic matter content and pH on the toxicity of ZnO nanoparticles to Folsomia candida. Ecotoxicol Environ Saf 108:9–15. https://doi.org/10.1016/j.ecoenv.2014.06.031
Williams AP, Abatzoglou JT, Gershunov A, Guzman-Morales J, Bishop DA, Balch JK, Lettenmaier DP (2019) Observed impacts of anthropogenic climate change on wildfire in California. Earth's Future 7:892–910. https://doi.org/10.1029/2019EF001210
Ying GG, Kookana RS (2001) Sorption of fipronil and its metabolites on soils from South Australia. J Environ Sci Heal Part B Pesdtic Food Contam Agric Wastes 36:545–558. https://doi.org/10.1081/PFC-100106184
Zortéa T, da Silva AS, dos Reis TR, Segat JC, Paulino AT, Sousa JP, Baretta D (2018a) Ecotoxicological effects of fipronil, neem cake and neem extract in edaphic organisms from tropical soil. Ecotoxicol Environ Saf 166:207–214. https://doi.org/10.1016/j.ecoenv.2018.09.061
Zortéa T, dos Reis TR, Serafini S, de Sousa JP, da Silva AS, Baretta D (2018b) 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
Thanks are due to Dr. Luiz Antonio Martinelli, Dr. Janaina Braga do Carmo and Dr. Leonardo Machado Pitombo for their technical contribution to the measurement of the physical-chemical parameters of the natural soil used. The authors also thank the Brazilian coordination of Superior Level Staff Improvement (CAPES) for the master’s degree scholarship conceded and the São Paulo Research Foundation (FAPESP) for the financial support conceded via the thematic project “Environmental Effects of the Pasture-Sugarcane Conversion and Pasture Intensification” (Process: 2015/187903) and the post-doctoral grant (Process PDJ: 2017/04858-0).
Funding
This work was supported by the Brazilian coordination of Superior Level Staff Improvement (CAPES) through a master degree scholarship attributed to Maria Carolina Triques and by the São Paulo Research Foundation (FAPESP) through financial support conceded via the thematic project “Environmental Effects of the Pasture-Sugarcane Conversion and Pasture Intensification” (Process: 2015/187903) and through post-doctoral grant conceded to Vanessa Bezerra de Menezes-Oliveira (Process PDJ: 2017/04858–0).
Author information
Authors and Affiliations
Contributions
MCT conceptualization, methodology, formal analysis, investigation, and writing (Original draft); FR investigation, formal analysis, writing and editing, (Original draft); DO conceptualization, methodology, formal analysis, and investigation; BVGt methodology and investigation; CCM article investigation and resources; ELGE investigation, resources, and supervision; VB de M-O article conceptualization, methodology, formal analysis, investigation, writing (Original draft and review), resources and supervision.
Corresponding author
Ethics declarations
Competing Interests
The authors have no relevant financial or non-financial interests to disclose.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Triques, M.C., Ribeiro, F., de Oliveira, D. et al. The Ecotoxicity of Sugarcane Pesticides to Non-target Soil Organisms as a Function of Soil Properties and Moisture Conditions. Int J Environ Res 16, 61 (2022). https://doi.org/10.1007/s41742-022-00433-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s41742-022-00433-6