Effects of realistic pesticide mixtures on the springtail Folsomia candida

. 2025 May 01 ; 44 (5) : 1347-1356.

Jazyk angličtina Země Velká Británie, Anglie Médium print

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40037586

Grantová podpora
SPRINT
European Commission through Horizon 2020
862568 European Union Research and Innovation Programme

The application of multiple pesticides over the last decades has resulted in their frequent and in some cases long-term presence in soils as complex mixtures. This work assessed the toxicity of realistic pesticide mixtures to the springtail Folsomia candida observed in 11 case study sites. Each mixture was composed of five pesticides (as active substances or metabolites), chosen based on their occurrence in soil and expected risk to soil invertebrates. Reproduction tests were conducted in natural agricultural soil, and the springtails were exposed to three concentrations of the selected pesticides: the median environmental concentration (MEC), the predicted environmental concentration (PEC), and five times PEC (5PEC). No significant effect was observed at MEC exposure in any case study sites; however, effects on reproduction, adult survival, and adult size were observed at PEC and 5PEC exposures in five case study sites. Risk quotients (RQs) of individual pesticides were calculated by dividing the exposure concentrations (MEC, PEC, and 5PEC) by the no observed effect concentration values from the literature, and the sum of the five pesticides was calculated as ∑RQ in each case study site. The toxicity at PEC exposure was higher than expected based on the ∑RQ in two case study sites, indicating a possible synergistic mixture effect. This work provides new information on the effects of realistic pesticide mixtures. Further research is required to clarify whether the current risk assessment of individual pesticides adequately protects soil species from exposure to multiple pesticide residues that may occur in even more complex mixtures.

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Alves P. R. L., Cardoso E. J. B. N., Martines A. M., Sousa J. P., Pasini A. (2014). Seed dressing pesticides on springtails in two ecotoxicological laboratory tests. Ecotoxicology and Environmental Safety, 105, 65–71. 10.1016/j.ecoenv.2014.04.010 PubMed DOI

Alves P. R. L., de Araújo R. S., Ogliari Bandeira F., Matias W. G. (2023). Individual and combined toxicity of imidacloprid and two seed dressing insecticides on collembolans Folsomia candida. Journal of Toxicology and Environmental Health. Part A, 86, 166–179. 10.1080/15287394.2023.2174464 PubMed DOI

Amorim M. J. B., Pereira C., Menezes-Oliveira V. B., Campos B., Soares A. M. V. M., Loureiro S. (2012). Assessing single and joint effects of chemicals on the survival and reproduction of Folsomia candida (Collembola) in soil. Environmental Pollution, 160, 145–152. 10.1016/j.envpol.2011.09.005 PubMed DOI

Bakanov N., Honert C., Eichler L., Lehmann G. U. C., Schulz R., Brühl C. A. (2023). A new sample preparation approach for the analysis of 98 current-use pesticides in soil and herbaceous vegetation using HPLC-MS/MS in combination with an acetonitrile-based extraction. Chemosphere, 331, 138840. 10.1016/j.chemosphere.2023.138840 PubMed DOI

Bakker R., Ekelmans A., Xie L., Vooijs R., Roelofs D., Ellers J., Hoedjes K. M., van Gestel C. A. M. (2022). Biomarker development for neonicotinoid exposure in soil under interaction with the synergist piperonyl butoxide in Folsomia candida. Environmental Science and Pollution Research International, 29, 80897–80909. 10.1007/s11356-022-21362-z PubMed DOI PMC

Beaumelle L., Tison L., Eisenhauer N., Hines J., Malladi S., Pelosi C., Thouvenot L., Phillips H. R. P. (2023). Pesticide effects on soil fauna communities—A meta-analysis. Journal of Applied Ecology, 60, 1239–1253. 10.1111/1365-2664.14437 DOI

Bentley K. S., Fletcher J. L., Woodward M. D. (2010). Chlorantraniliprole: An insecticide of the anthranilic diamide class. In Hayes’ handbook of pesticide toxicology (3rd ed., Vol. 1, pp. 2231–2242). Academic Press. 10.1016/B978-0-12-374367-1.00102-6 DOI

Boye K., Lindström B., Boström G., Kreuger J. (2019). Long‐term data from the Swedish National Environmental Monitoring Program of Pesticides in Surface Waters. Journal of Environmental Quality, 48, 1109–1119. 10.2134/jeq2019.02.0056 PubMed DOI

Candolfi M. P., Barrett K. L., Cambell P. J., Forster R., Grandy N., Huet M.-C., Lewis G., Oomen P. A., Schmuck R., Vogt H. (2001). Guidance document on regulatory testing and risk assessment procedures for plant protection products with non target arthropods. In Proceedings from the ESCORT 2 workshop. Proceedings of the SETAC, Pensacola. (Vol. 46).

Capella R., Guida Y., Loretto D., Weksler M., Meire R. O. (2023). Occurrence of legacy organochlorine pesticides in small mammals from two mountainous national parks in southeastern Brazil. Emerging Contaminants, 9, 100211. 10.1016/j.emcon.2023.100211 DOI

Cedergreen N. (2014). Quantifying synergy: A systematic review of mixture toxicity studies within environmental toxicology. PloS One, 9, e96580. 10.1371/journal.pone.0096580 PubMed DOI PMC

Chandra R., Sharpanabharathi N., Prusty B. A. K., Azeez P. A., Kurakalva R. M. (2021). Organochlorine pesticide residues in plants and their possible ecotoxicological and agri food impacts. Scientific Reports, 11, 17841. 10.1038/s41598-021-97286-4 PubMed DOI PMC

Chow R., Scheidegger R., Doppler T., Dietzel A., Fenicia F., Stamm C. (2020). A review of long-term pesticide monitoring studies to assess surface water quality trends. Water Research X, (9, 100064. 10.1016/j.wroa.2020.100064 PubMed DOI PMC

de Lima e Silva C., van Haren C., Mainardi G., de Rooij W., Ligtelijn M., van Straalen N. M., van Gestel C. A. M. (2021). Bringing ecology into toxicology: Life-cycle toxicity of two neonicotinoids to four different species of springtails in LUFA 2.2 natural soil. Chemosphere, 263, 128245. 10.1016/j.chemosphere.2020.128245 PubMed DOI

European Commission. (2002). Guidance document on terrestrial ecotoxicology under Council Directive 91/414/EEC. In European Commission, Health & Consumer Protection Directorate-General—Guidance document on terrestrial ecotoxicology under Council Directive 91/414/EEC.

European Commission. (2009). Regulation (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. Official Journal of the European Union (Vol. 309, Issue 1). http://data.europa.eu/eli/reg/2009/1107/2022-11-21

European Commission. (2011). Commission Regulation (EU) No 546/2011 of 10 June 2011 implementing Regulation (EC) No 1107/2009 of the European Parliament and of the Council as regards uniform principles for evaluation and authorisation of plant protection products. http://data.europa.eu/eli/reg/2011/546/2022-11-21

European Commission. (2013a). Commission Regulation (EU) No 283/2013 of 1 March 2013 setting out the data requirements for active substances, in accordance with Regulation (EC) No 1107/2009 of the European Parliament and of the Council concerning the placing of plant protection producion. http://data.europa.eu/eli/reg/2013/283/2022-11-21

European Commission. (2013b). Commission Regulation (EU) No 284/2013 of 1 March 2013 setting out the data requirements for plant protection products, in accordance with Regulation (EC) No 1107/2009 of the European Parliament and of the Council concerning the placing of plant protection. http://data.europa.eu/eli/reg/2013/284/2022-11-21

European Commission. (2023a). Approval of active substances. https://food.ec.europa.eu/plants/pesticides/approval-active-substances_en

European Commission. (2023b). Authorisation of plant protection products. https://food.ec.europa.eu/plants/pesticides/authorisation-plant-protection-products_en

European Food Safety Authority. (2011). Conclusion on the peer review of the pesticide risk assessment of the active substance difenoconazole. EFSA Journal, 9, 1967. 10.2903/j.efsa.2011.1967] DOI

European Food Safety Authority. (2013). Conclusion on the peer review of the pesticide risk assessment of the active substance chlorantraniliprole. EFSA Journal, 11, 3143. 10.2903/j.efsa.2013.3143 DOI

European Food Safety Agency. (2023). How Europe ensures pesticides are safe. https://multimedia.efsa.europa.eu/pesticides-authorisation/index.htm

Food and Agriculture Organization of the United Nations. (2022). Pesticides use, pesticides trade and pesticides indicators—Global, regional and country trends, 1990–2020. FAOSTAT Analytical Briefs, No. 46.

Ferreira P., Gabriel A., Sousa J. P., Natal-da-Luz T. (2022). Representativeness of Folsomia candida to assess toxicity of a new generation insecticide in different temperature scenarios. The Science of the Total Environment, 837, 155712. 10.1016/j.scitotenv.2022.155712 PubMed DOI

Frische T., Matezki S., Wogram J. (2014). Environmental risk assessment of pesticide mixtures under regulation 1107/2009/EC: A regulatory review by the German Federal Environment Agency (UBA). Journal Für Verbraucherschutz Und Lebensmittelsicherheit, 9, 377–389. 10.1007/s00003-014-0916-6 DOI

Froger C., Jolivet C., Budzinski H., Pierdet M., Caria G., Saby N. P. A., Arrouays D., Bispo A. (2023). Pesticide residues in French soils: Occurrence, risks, and persistence. Environmental Science & Technology, 57, 7818–7827. 10.1021/acs.est.2c09591 PubMed DOI PMC

Geissen V., Silva V., Lwanga E. H., Beriot N., Oostindie K., Bin Z., Pyne E., Busink S., Zomer P., Mol H., Ritsema C. J. (2021). Cocktails of pesticide residues in conventional and organic farming systems in Europe—Legacy of the past and turning point for the future. Environmental Pollution, 278, 116827. 10.1016/j.envpol.2021.116827 PubMed DOI

Goscinny S., Unterluggauer H., Aldrian J., Hanot V., Masselter S. (2012). Determination of glyphosate and its metabolite AMPA (aminomethylphosphonic acid) in cereals after derivatization by isotope dilution and UPLC-MS/MS. Food Analytical Methods, 5, 1177–1185. 10.1007/s12161-011-9361-7 DOI

Gunstone T., Cornelisse T., Klein K., Dubey A., Donley N. (2021). Pesticides and soil invertebrates: A hazard assessment. Frontiers in Environmental Science, 9, 643847. 10.3389/fenvs.2021.643847 DOI

Haas J., Glaubitz J., Koenig U., Nauen R. (2022). A mechanism-based approach unveils metabolic routes potentially mediating chlorantraniliprole synergism in honey bees, Apis mellifera L., by azole fungicides. Pest Management Science, 78, 965–973. 10.1002/ps.6706 PubMed DOI PMC

Herrero-Hernández E., Simón-Egea A. B., Sánchez-Martín M. J., Rodríguez-Cruz M. S., Andrades M. S. (2020). Monitoring and environmental risk assessment of pesticide residues and some of their degradation products in natural waters of the Spanish vineyard region included in the Denomination of Origin Jumilla. Environmental Pollution, 264, 114666. 10.1016/j.envpol.2020.114666 PubMed DOI

Hester K. P., Stoner K. A., Eitzer B. D., Koethe R. W., Lehmann D. M. (2023). Pesticide residues in honey bee (Apis mellifera) pollen collected in two ornamental plant nurseries in Connecticut: Implications for bee health and risk assessment. Environmental Pollution, 333, 122037. 10.1016/j.envpol.2023.122037 PubMed DOI PMC

Hvězdová M., Kosubová P., Košíková M., Scherr K. E., Šimek Z., Brodský L., Šudoma M., Škulcová L., Sáňka M., Svobodová M., Krkošková L., Vašíčková J., Neuwirthová N., Bielská L., Hofman J. (2018). Currently and recently used pesticides in Central European arable soils. Science of the Total Environment, 613-614, 361–370. 10.1016/j.scitotenv.2017.09.049 PubMed DOI

Jegede O., Tourinho P. S., Geissen V., Hofman J. (2024). Prioritization of currently used pesticides in soils of main European cropping systems and an Argentinian cropping system for assessment of mixture toxicity and risk on terrestrial biota. preprint: not peer reviewed. 10.2139/ssrn.4871771 DOI

Joimel S., Chassain J., Artru M., Faburé J. (2022). Collembola are among the most pesticide-sensitive soil fauna groups: A meta-analysis. Environmental Toxicology and Chemistry, 41, 2333–2341. 10.1002/etc5428 PubMed DOI PMC

Kaczyński P., Łozowicka B. (2015). Liquid chromatographic determination of glyphosate and aminomethylphosphonic acid residues in rapeseed with MS/MS detection or derivatization/fluorescence detection. Open Chemistry, 13 000010151520150107. 10.1515/chem-2015-0107 DOI

Knuth D., Gai L., Silva V., Harkes P., Hofman J., Šudoma M., Bílková Z., Alaoui A., Mandrioli D., Pasković I., Polić Pasković M., Baldi I., Bureau M., Alcon F., Contreras J., Glavan M., Abrantes N., Campos I., Norgaard T., Geissen V. (2024). Pesticide residues in organic and conventional agricultural soils across Europe: Measured and predicted concentrations. Environmental Science & Technology, 58, 6744–6752. PubMed PMC

Kosubová P., Škulcová L., Poláková Š., Hofman J., Bielská L. (2020). Spatial and temporal distribution of the currently-used and recently-banned pesticides in arable soils of the Czech Republic. Chemosphere, 254, 126902. 10.1016/j.chemosphere.2020.126902 PubMed DOI

Kuang L., Hou Y., Huang F., Guo A., Deng W., Sun H., Shen L., Lin H., Hong H. (2020). Pesticides in human milk collected from Jinhua, China: Levels, influencing factors and health risk assessment. Ecotoxicology and Environmental Safety, 205, 111331. 10.1016/j.ecoenv.2020.111331 PubMed DOI

Lavtižar V., Berggren K., Trebše P., Kraak M. H. S., Verweij R. A., van Gestel C. A. M. (2016). Comparative ecotoxicity of chlorantraniliprole to non-target soil invertebrates. Chemosphere, 159, 473–479. 10.1016/j.chemosphere.2016.06.036 PubMed DOI

Mark J., Fantke P., Soheilifard F., Alcon F., Contreras J., Abrantes N., Campos I., Baldi I., Bureau M., Alaoui A., Christ F., Mandrioli D., Sgargi D., Pasković I., Pasković M. P., Glavan M., Hofman J., Harkes P., Lwanga E. H., Tamm L. (2024). Selected farm-level crop protection practices in Europe and Argentina: Opportunities for moving toward sustainable use of pesticides. Journal of Cleaner Production, 477, 143577. 10.1016/j.jclepro.2024.143577 DOI

Mekonen S., Belete B., Melak F., Ambelu A. (2023). Determination of pesticide residues in the serum of flower farm workers: A growing occupational hazards in low income countries. Toxicology Reports, 10, 293–300. 10.1016/j.toxrep.2023.02.012 PubMed DOI PMC

Moore D. R. J., Caux P. Y. (1997). Estimating low toxic effects. Environmental Toxicology and Chemistry, 16, 794–801. 10.1002/etc5620160425 DOI

Organisation for Economic Co-operation and Development. (2009). OECD Guidelines for the testing of chemicals - 232 Collembolan reproduction test in soil.

Ogle D., Doll J., Wheeler A., Dinno A. (2023). FSA: Simple fisheries stock assessment methods. R package version 0.9.5. https://cran.r-project.org/package=FSA

Panico S. C., van Gestel C. A. M., Verweij R. A., Rault M., Bertrand C., Menacho Barriga C. A., Coeurdassier M., Fritsch C., Gimbert F., Pelosi C. (2022). Field mixtures of currently used pesticides in agricultural soil pose a risk to soil invertebrates. Environmental Pollution, 305, 119290. 10.1016/j.envpol.2022.119290 PubMed DOI

Pelosi C., Bertrand C., Daniele G., Coeurdassier M., Benoit P., Nélieu S., Lafay F., Bretagnolle V., Gaba S., Vulliet E., Fritsch C. (2021). Residues of currently used pesticides in soils and earthworms: A silent threat? Agriculture, Ecosystems and Environment, 305, 107167. 10.1016/j.agee.2020.107167 DOI

Pitombeira de Figueirêdo L., Athayde D. B., Daam M. A., van Gestel C. A. M., Guerra G., da S., Duarte-Neto P. J., Espíndola E. L. G. (2020). Impact of temperature on the toxicity of Kraft 36 EC® (a.s. abamectin) and Score 250 EC® (a.s. difenoconazole) to soil organisms under realistic environmental exposure scenarios. Ecotoxicology and Environmental Safety, 194, 110446. 10.1016/j.ecoenv.2020.110446 PubMed DOI

Pitombeira de Figueirêdo L., Daam M. A., Mainardi G., Mariën J., Espíndola E. L. G., van Gestel C. A. M., 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. Environmental Pollution, 244, 342–350. 10.1016/j.envpol.2018.10.077 PubMed DOI

Santos M. J. G., Soares A. M. V. M., Loureiro S. (2010). Joint effects of three plant protection products to the terrestrial isopod Porcellionides pruinosus and the collembolan Folsomia candida. Chemosphere, 80, 1021–1030. 10.1016/j.chemosphere.2010.05.031 PubMed DOI

Servicio Nacional de Sanidad y Calidad Agroalimentaria. (2024). National registry of plant therapeutics. https://aps2.senasa.gov.ar/vademecum/app/publico

Silva V., Alaoui A., Schlünssen V., Vested A., Graumans M., van Dael M., Trevisan M., Suciu N., Mol H., Beekmann K., Figueiredo D., Harkes P., Hofman J., Kandeler E., Abrantes N., Campos I., Martínez M. Á., Pereira J. L., Goossens D., Scheepers P. T. J. (2021). Collection of human and environmental data on pesticide use in Europe and Argentina: Field study protocol for the SPRINT project. PloS One, 16, e0259748. 10.1371/journal.pone.0259748 PubMed DOI PMC

Silva V., Gai L., Harkes P., Tan G., Ritsema C. J., Alcon F., Contreras J., Abrantes N., Campos I., Baldi I., Bureau M., Christ F., Mandrioli D., Sgargi D., Pasković I., Polić Pasković M., Glavan M., Hofman J., Huerta Lwanga E., Geissen V. (2023). Pesticide residues with hazard classifications relevant to non-target species including humans are omnipresent in the environment and farmer residences. Environment International, 181, 108280. 10.1016/j.envint.2023.108280 PubMed DOI

Silva V., Mol H. G. J., Zomer P., Tienstra M., Ritsema C. J., Geissen V. (2019). Pesticide residues in European agricultural soils—A hidden reality unfolded. Science of the Total Environment, 653, 1532–1545. 10.1016/j.scitotenv.2018.10.441 PubMed DOI

Souza R. C., Portella R. B., Almeida P. V. N. B., Pinto C. O., Gubert P., Santos da Silva J. D., Nakamura T. C., do Rego E. L. (2020). Human milk contamination by nine organochlorine pesticide residues (OCPs). Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes, 55, 530–538. 10.1080/03601234.2020.1729630 PubMed DOI

Szabó B., Révész A., Boros G. (2023). Additive and dose-dependent mixture effects of Flumite 200 (flufenzin, acaricide) and Quadris (azoxystrobin, fungicide) on the reproduction and survival of Folsomia candida (Collembola). Ecotoxicology and Environmental Safety, 263, 115219. 10.1016/j.ecoenv.2023.115219 PubMed DOI

Tongo I., Onokpasa A., Emerure F., Balogun P. T., Enuneku A. A., Erhunmwunse N., Asemota O., Ogbomida E., Ogbeide O., Ezemonye L. (2022). Levels, bioaccumulation and biomagnification of pesticide residues in a tropical freshwater food web. International Journal of Environmental Science and Technology, 19, 1467–1482. 10.1007/s13762-021-03212-6 DOI

van Gestel C. A. M. (2012). Soil ecotoxicology: State of the art and future directions. ZooKeys, 176, 275–296. PubMed PMC

Weisner O., Frische T., Liebmann L., Reemtsma T., Roß-Nickoll M., Schäfer R. B., Schäffer A., Scholz-Starke B., Vormeier P., Knillmann S., Liess M. (2021). Risk from pesticide mixtures—The gap between risk assessment and reality. Science of the Total Environment, 796, 149017. 10.1016/j.scitotenv.2021.149017 PubMed DOI

Yang X., Wang F., Bento C. P. M., Xue S., Gai L., van Dam R., Mol H., Ritsema C. J., Geissen V. (2015). Short-term transport of glyphosate with erosion in Chinese loess soil—A flume experiment. Science of the Total Environment, 512-513, 406–414. 10.1016/j.scitotenv.2015.01.071 PubMed DOI

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