Abstract
This study assessed the influence of three tropical soil types and soil moisture content on the toxicity and risk of the insecticide fipronil to collembolans Folsomia candida. Chronic toxicity tests were performed in a Tropical Artificial Soil (TAS), an Oxisol and an Entisol spiked with increasing concentrations of fipronil to assess the effects on the reproduction and growth of the species. The soil moisture contents were kept at 60% (standard condition) and 30 or 45% (water restriction) of their water holding capacity (WHC). The toxicity of fipronil on collembolans reproduction was about three times higher in Entisol compared to TAS or Oxisol. Higher toxicities were also found in the drier TAS (EC50 30%WHC = 0.20 vs EC50 60%WHC = 0.70 mg kg−1) and Oxisol (EC50 45%WHC = 0.27 vs EC50 60%WHC = 0.54 mg kg−1), while in Entisol lower impacts were found in the drier samples (EC50 30%WHC = 0.41 vs EC50 60%WHC = 0.24 mg kg−1). For all tested soils, the size of generated collembolans was reduced by the fipronil concentrations, regardless of soil moisture. However, the drier condition increased the effect on the growth in TAS and Entisol for some concentrations. A significant risk of exposure was found in TAS and Oxisol at drier conditions and, for Entisol, regardless of the soil moisture. The toxic effects and risk of fipronil on collembolans were higher in the natural sandy soil. The soil moisture content increase or decrease the toxicity of the insecticide for collembolans, depending on soil type.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available and should be requested by e-mail.
Code availability
ImageJ, RRID:SCR_003070; STATISTICA, RRID:SCR_014213; SCAPE, RRID: Not available.
References
Alves PRL, Cardoso EJBN, Martines AM, Sousa JP, Pasini A (2013) Earthworm ecotoxicological assessments of pesticides used to treat seeds under tropical conditions. Chemosphere 90:2674–2682. https://doi.org/10.1016/j.chemosphere.2012.11.046
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
Alves PRL, Bandeira FO, Presotto R, Giraldi M, Segat JC, Cardoso EJBN, Baretta D (2019) Ecotoxicological assessment of Fluazuron: effects on Folsomia candida and Eisenia andrei. Environ Sci Pollut Res 26:5842–5850. https://doi.org/10.1007/s11356-018-4022-7
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
Bandeira FO, Alves PRL, Hennig TB, Schiehl A, Cardoso EJBN, Baretta D (2019) Toxicity of imidacloprid to the earthworm Eisenia andrei and collembolan Folsomia candida in three contrasting tropical soils. J Soils Sediments 20:1997–2007. https://doi.org/10.1007/s11368-019-02538-6
Bandeira FO, Alves PRL, Hennig TB, Toniolo T, Natal-da-Luz T, Baretta D (2020) Effect of temperature on the toxicity of imidacloprid to Eisenia andrei and Folsomia candida in tropical soils. Environ Pollut 267:115565. https://doi.org/10.1016/j.envpol.2020.115565
Bandow C, Coors A, Karau N, Römbke J (2014a) Interactive effects of lambda-cyhalothrin, soil moisture and temperature on Folsomia candida and Sinella curviseta (Collembola). Environ Toxicol Chem 33:654–661. https://doi.org/10.1002/etc.2479
Bandow C, Karau N, Römbke J (2014b) 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
Bandow C, Ng EL, Schmelz RM, Sousa JP, Römbke J (2016) A TME study with the fungicide pyrimethanil combined with different moisture regimes: effects on enchytraeids. Ecotoxicology 25:213–224. https://doi.org/10.1007/s10646-015-1581-y
Bobé A, Coste CM, Cooper JF (1997) Factors Influencing the Adsorption of Fipronil on Soils. J Agric Food Chem 45:4861–4865. https://doi.org/10.1021/jf970362z
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
Brodeur JC, Sanchez M, Castro L, Rojas DE, Cristos D, Damonte MJ, Poliserpi MB, D’Andrea MF, Andriulo AE (2017) Accumulation of current-use pesticides, cholinesterase inhibition and reduced body condition in juvenile one-sided livebearer fish (Jenynsia multidentata) from the agricultural Pampa region of Argentina. Chemosphere 185:36–46. https://doi.org/10.1016/j.chemosphere.2017.06.129
Bursell E (1970) An introduction to insect physiology. Academic Press, London, UK, p 276
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
Cary TL, Chandler GT, Volz DC, Walse SS, Ferry JL (2004) Phenylpyrazole Insecticide Fipronil Induces Male Infertility in the Estuarine Meiobenthic Crustacean Amphiascus tenuiremis. Environ Sci Technol 38:522–528. https://doi.org/10.1021/es034494m
Chelinho S, Domene X, Campana P, Andrés P, Römbke J, Sousa JP (2014) Toxicity of phenmedipham and carbendazim to Enchytraeus crypticus and Eisenia andrei (Oligochaeta) in Mediterranean soils. J Soils Sediments 14:584–599. https://doi.org/10.1007/s11368-013-0818-8
Coleman DC, Crossley DA, Hendrix PF (2004) Fundamentals of Soil Ecology, 2nd ed. Elsevier Inc, Athens, Georgia, p 502
Crouau Y, Chenon P, Gisclard C (1999) The use of Folsomia candida (Collembola, Isotomidae) for the bioassay of xenobiotic substances and soil pollutants. Appl Soil Ecol 12:103–111. https://doi.org/10.1016/S0929-1393(99)00002-5
Culik MP, Zeppelini FD (2003) Diversity and distribution of Collembola (Arthropoda: Hexapoda) of Brazil. Biodivers Conserv 12:1119–1143. https://doi.org/10.1023/A:1023069912619
Daam MA, Chelinho S, Niemeyer JC, Owojori OJ, De Silva PMCS, Sousa JP, van Gestel CAM, Römbke J (2019) Environmental risk assessment of pesticides in tropical terrestrial ecosystems: test procedures, current status and future perspectives. Ecotoxicol Environ Saf 181:534–547. https://doi.org/10.1016/j.ecoenv.2019.06.038
Da Silva KMD, Rezende LCSH, Bergamasco R, Da Silva CA, Gonçalves DS (2012) Caracterização Físico - Química Da Fibra De Coco Verde Para a Adsorção De Metais Pesados Em Efluente De Indústria De Tintas. Engevista 15:43. https://doi.org/10.22409/engevista.v15i1.387
Domene X, Colón J, Uras MV, Izquierdo R, Àvila A, Alcañiz JM (2010) Role of soil properties in sewage sludge toxicity to soil collembolans. Soil Biol Biochem 42:1982–1990. https://doi.org/10.1016/j.soilbio.2010.07.019
Domene X, Chelinho S, Campana P, Natal-da-Luz T, Alcañiz JM, Andrés P, Römbke J, Sousa JP (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
Domene X, Römbke J, Chelinho S, Sousa JP, Campana P, Alcañiz JM (2012) Applying a GLM-based approach to model the influence of soil properties on the toxicity of phenmedipham to Folsomia candida. J. Soils Sediments 12:888–899. https://doi.org/10.1007/s11368-012-0502-4
EC - European Commission (2002) Guidance Document on Terrestrial Ecotoxicology under Council Directive 91/414/EEC (SANCO/10329/2002) rev.2 final, 17.10.2002, p. 1 - 39
Edney EB (1977) Water balance in land arthropods. Springer-Verlag, Berlin, Germany, p 282
EFSA - European Food Safety Authority (2006) Conclusion regarding the peer review of the pesticide risk assessment of the active substance metazachlor. EFSA J 6:1–110. https://doi.org/10.2903/j.efsa.2008.145r
EMBRAPA - Empresa Brasileira de Pesquisa Agropecuária (1988) Recomendações técnicas para o cultivo da soja. Circular técnica 16. Unidade de execução de pesquisa de âmbito estadual de Dourados, MS. Dourados
EMBRAPA (2006) Ata da XXVII Reunião de Pesquisa de Soja da Região Central do Brasil. Embrapa Soja, Londrina, Brazil.lSSN 1516-781X: n. 265
Environmental Canada (2007) Guidance Document on Statistical Methods for Environmental Toxicity Test. Environmental Protection Series, EPS 1/RM/46, 2005 with 2007 updates. Environmental Canada, Ottawa
EPPO - European and Mediterranean Plant Protection Organization (2003) Environmental risk assessment scheme for plant protection products. Chapter 4: Soil. OEPP EPP0 Bull 33:151–162
ESCAPE (2013) ESCAPE 2.0v: Estimation of soil concentrations after pesticide applications. Fraunhofer IME, Aachen, Germany
Fishel F (2003) Pesticides and the Environment. Agricultural MU Guide (Insects and Diseases), University of Missouri, Columbia, United States of America
Gaertner K, Chandler GT, Quattro J, Ferguson PL, Sabo-Attwood T (2012) Identification and expression of the ecdysone receptor in the harpacticoid copepod, Amphiascus tenuiremis, in response to fipronil. Ecotoxicol Environ Saf 76:39–45. https://doi.org/10.1016/j.ecoenv.2011.09.008
Garcia MVB (2004) Effects of pesticides on soil fauna: development of ecotoxicological test methods for tropical regions. Ecology and development series, vol. 19. Doctoral thesis, University of Bonn, Bonn, Germany
Gebrehiwot WH, Erkmen C, Uslu B (2019) A novel HPLC-DAD method with dilute-and-shoot sample preparation technique for the determination of buprofezin, dinobuton and chlorothalonil in food, environmental and biological samples. J IAEAC 99:1–15. https://doi.org/10.1080/03067319.2019.1702169
Guimarães B, Maria VL, Römbke J, Amorim MJB (2019) Exposure of Folsomia candida (Willem 1902) to teflubenzuron over three generations – Increase of toxicity in the third generation. Appl Soil Ecol 134:8–14. https://doi.org/10.1016/j.apsoil.2018.10.003
Gunasekara A, Truong T, Goh KS, Spurlock F, Tjeerdema RR (2007) Environmental fate and toxicology of fipronil. J Pestic Sci 32(3):189–199. https://doi.org/10.1584/jpestics.R07-02
Harris CR (1964) Influence of soil type and soil moisture on the toxicity of insecticides in soils to insects. Nature 202:724
Hennig TB, Bandeira FO, Dalpasquale AJ, Cardoso EJBN, Baretta D, Alves PRL (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
Hoffmann AA, Sørensen JG, Loeschcke V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J Therm Biol 28:175–216
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
IBAMA - Instituto brasileiro do meio ambiente e dos recursos naturais renováveis - IBAMA (1996) Normative Ordinance No. 84, October 15th, 1996. Establish Procedures to Be Adopted in the Brazilian Institute of Environment and Renewable Natural Resources e IBAMA, for Registration Purposes and for Assessment of the Potential Environmental Hazard (PPA) of Pesticides, vol. 203. Union Official Journal No, p. 21358, 1996. Brasília, Brazil (in Portuguese)
INMETRO - Instituto Nacional de Metrologia, Qualidade e Tecnologia (2020) Orientações sobre Validação de Métodos Analíticos: DOQ-CGCRE-008. Rev. 09 de jun 2020. Brasília, Brazil, p. 1 - 30. Available at: https://www.inmetro.gov.br/Sidoq/pesquisa_link.asp?seq_tipo_documento=5&cod_uo_numeracao=00774&num_documento=008. Accessed 06 August 2021.
IPCC - Intergovernmental Panel on Climate Change (2014) In: Pachauri, R.K., Meyer, L.A. (eds), Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team]. IPCC, Geneva, Switzerland
ISO - International Organization for Standardization (2014) Soil quality: Inhibition of reproduction of Collembola (Folsomiacandida) by soil contaminants. ISO, Geneva, Switzerland
Jackson D, Cornell CB, Luukinen B, Buhl K, Stone D (2009) Fipronil Technical Fact Sheet; National Pesticide Information Center, Oregon State University Extension Services, Oregon, United States of America
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
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
Li M, Li P, Wang L, Feng M, Han L (2015) Determination and dissipation of fipronil and its metabolites in peanut and soil. J Agric Food Chem 63:4435–4443. https://doi.org/10.1021/jf5054589
Lima MPR, Soares AMVM, Loureiro S (2011) Combined effects of soil moisture and carbaryl to earthworms and plants: Simulation of flood and drought scenarios. Environ Pollut 159:1844–1851. https://doi.org/10.1016/j.envpol.2011.03.029
Maccari AP, Baretta D, Paiano D, Leston S, Freitas A, Ramos F, Sousa JP, Klauberg-Filho O (2016) Ecotoxicological effects of pig manure on Folsomia candida in subtropical Brazilian soils. J Hazard Mater 314:113–120. https://doi.org/10.1016/j.jhazmat.2016.04.013
Mandal K, Singh B (2013) Persistence of fipronil and its metabolites in sandy loam and clay loam soils under laboratory conditions. Chemosphere 91:1596–1603. https://doi.org/10.1016/j.chemosphere.2012.12.054
Masutti CSM, Mermut AR (2007) Degradation of fipronil under laboratory conditions in a tropical soil from sirinhaém Pernambuco, Brazil. J Environ Sci Heal - Part B Pestic Food Contam Agric Wastes 42:33–43. https://doi.org/10.1080/03601230601017981
Mohapatra S, Deepa M, Rashmi N, Jagdish GK, Kumar S, Prakash GS (2010) Fate of Fipronil and its Metabolites in/on Grape Leaves, Berries and Soil Under Semi Arid Tropical Climatic Conditions. Bull Environ Contam Toxicol 84:587–591. https://doi.org/10.1007/s00128-010-9965-4
Niemeyer JC, Carniel LSC, de Santo FB, Silva M, Klauberg-Filho O (2018) Boric acid as reference substance for ecotoxicity tests in tropical artificial soil. Ecotoxicology 27:395–401. https://doi.org/10.1007/s10646-018-1915-7
Ogungbemi AO, Van Gestel CAM (2018) Extrapolation of imidacloprid toxicity between soils by exposing Folsomia candida in soil pore water. Ecotoxicology 27:1107–1115. https://doi.org/10.1007/s10646-018-1965-x
PBMC (2014) Base científica das mudanças climáticas. Contribuição do Grupo de Trabalho 1 do Painel Brasileiro de Mudanças Climáticas ao Primeiro Relatório da Avaliação Nacional sobre Mudanças Climáticas [Ambrizzi, T., Araujo, M. (eds.)]. COPPE. Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brasil, p 464
Peijnenburg W, Capri E, Kula C, Liess M, Luttik R, Montforts M (2012) Technology Evaluation of Exposure Metrics for Effect Assessment of Soil Invertebrates. Crit Rev Env Sci Tec 42:17, 1862-1893. https://doi.org/10.1080/10643389.2011.574100
Ribeiro S, Sousa JP, Nogueira AJA (2001) Effect of endosulfan and parathion on energy reserves and physiological parameters of the terrestrial isopod Porcellio dilatatus. Ecotoxicol Environ Saf 49:131–138
San Miguel A, Raveton M, Lempérière G, Ravanel P (2008) Phenylpyrazoles impact on Folsomia candida (Collembola). Soil Biol Biochem 40:2351–2357. https://doi.org/10.1016/j.soilbio.2008.05.014
Scorza Jr RP, Frando AA (2013) A temperatura e umidade na degradação de fi pronil em dois solos de Mato Grosso do Sul. Ciência Rural 43:1203–1209
Segat JC, Alves PRL, Baretta D, Cardoso EJBN (2015) Ecotoxicological evaluation of swine manure disposal on tropical soils in Brazil. Ecotoxicol Environ Saf 122:91–97. https://doi.org/10.1016/j.ecoenv.2015.07.017
Silva RO, Scorza Jr RP, Bonfá MRL, Campanari MFZ, Mendes I, de C (2016) Degradation and sorption of fipronil and atrazine in Latossols with organic residues from sugarcane crop. Ciência Rural 46:1172–1177. https://doi.org/10.1590/0103-8478cr20150696
Singh A, Srivastava A, Srivastava PC (2014) Sorption kinetics of fipronil on soils. Bull Environ Contam Toxicol 93:758–763. https://doi.org/10.1007/s00128-014-1391-6
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
Singh J, Schälder M, Demetrio W, et al. (2019) Climate change effects on earthworms—a review. Soil Organisms 3:113–137. (ISSN 2509-9523 (online)). https://doi.org/10.25674/so91iss3pp114
Sławski M, Sławska M (2020) Collembolan Assemblages Response to Wild Boars (Sus scrofa L.) Rooting in Pine Forest Soil. Forests 11(11):1123. https://doi.org/10.3390/f11111123
Smit CE, Van Gestel CAM (1998) Effects of soil type, prepercolation, and ageing on bioaccumulation and toxicity of zinc for the springtail Folsomia candida. Environ Toxicol Chem 17:1132–1141. https://doi.org/10.1002/etc.5620170621
Sousa JP, Loureiro S, Pieper S, Frost M, Kratz W, Nogueira AJA, Soares AMVM (2000) Toxicokinetics of hydrophobic compounds in isopods. The importance of exposure route on the uptake of Lindane. Environ Toxicol Chem 19:2563–2577
Souza ED, Carneiro MAC, Paulino HB (2005) Physical attributes of a Typic Quartzipisamment and a Rhodic Hapludox under different management systems. Pesquisa Agropecuaria Brasileira 40:1135–1139. https://doi.org/10.1590/S0100-204X2005001100012
Spomer NA, Kamble ST (2010) Sorption and Desorption of Fipronil in Midwestern Soils. Bull Environ Contam Toxicol 84:264–268. https://doi.org/10.1007/s00128-009-9915-1
Szabó B, Seres A, Bakonyi G (2020) Distinct changes in the life-history strategies of Folsomia candida Willem (Collembola: Isotomidae) due to multi- and transgenerational treatments with an insecticide. App Soil Ecol 152:103563. https://doi.org/10.1016/j.apsoil.2020.103563
Tedesco MJ, Gianello C, Bissani CA, Bohnen H, Volkweiss SJ (1995) Análise de solo, plantas e outros materiais, 2nd edn. Universidade Federal do Rio Grande do Sul, Porto Alegre, p 147 (Boletim Técnico, 5)
Tingle CC, Rother JA, Dewhust CF, Lauer S, King WJ (2003) Fipronil: Environmental Fate, Ecotoxicology, and Human Health Concerns. Rev Environ Contam Toxicol 176:1–66
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
Van Gestel CAM (2012) Soil ecotoxicology: state of the art and future directions. Zookeys 176:275–296. https://doi.org/10.3897/zookeys.176.2275
Ying GG, Kookana RS (2006) Persistence and movement of fipronil termiticide with under-slab and trenching treatments. Environ Toxicol Chem 25:2045–2050. https://doi.org/10.1897/05-652R.1
Zortéa T, dos Reis TR, Serafini S, de Sousa JP, da Silva AS, Baretta D (2018a) 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
Zortéa T, da Silva AS, dos Reis TR, Segat JC, Paulino AT, Sousa JP, Baretta D (2018b) 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
Acknowledgements
The authors thank the National Council for Scientific and Technological Development (CNPq) for the research grant (Project 407170/2016-2). DB thanks the CNPq for the Research Productivity Grant (CNPq 305939/2018-1). TT and WES thanks the CNPq for a Grant of Scientific Initiation (process numbers 160246/2019-9 and 103524/2020-7, respectively). FOB and TBH thanks the Coordination for the Improvement of Higher Education Personnel (CAPES) for their master grant (process numbers 1735590 and 88882.447285/2019-01, respectively).
Author contributions
TBH: Conceptualization, Data curation, Formal analysis, Investigation, Writing—original draft. PRLA: Conceptualization, Formal analysis, Funding acquisition, Investigation, Project administration, Resources, Supervision, Writing—review & editing. TT: Investigation, Formal analysis. FOB: Investigation, Data curation, Formal analysis. WES: Investigation. LCC: Investigation, Data curation, Formal analysis. IKG: Investigation. DB: Resources, Supervision, Writing—review & editing.
Funding
This study was supported by the National Council for Scientific and Technological Development (CNPq) for the research grant (Project 407170/2016-2).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (Brazilian regimentation for the scientific use of animals - Law no. 11.794).
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
Hennig, T.B., Alves, P.R.L., Toniolo, T. et al. Toxicity of fipronil to Folsomia candida in contrasting tropical soils and soil moisture contents: effects on the reproduction and growth. Ecotoxicology 31, 64–74 (2022). https://doi.org/10.1007/s10646-021-02490-7
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-021-02490-7