Low concentrations of acetamiprid, deltamethrin, and sulfoxaflor, three commonly used insecticides, adversely affect ant queen survival and egg laying

. 2023 Sep 09 ; 13 (1) : 14893. [epub] 20230909

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37689830
Odkazy

PubMed 37689830
PubMed Central PMC10492783
DOI 10.1038/s41598-023-42129-7
PII: 10.1038/s41598-023-42129-7
Knihovny.cz E-zdroje

Ants are key ecosystem service providers and can serve as important biological control agents in pest management. However, the effects of insecticides on common farmland ant species are poorly understood. We tested the effects of three commonly used insecticides on ants (Hymenoptera, Formicidae). The tested insecticides were acetamiprid (neonicotinoid; formulated as Mospilan 20 SP), deltamethrin (pyrethroid; formulated as Sanium Ultra), and sulfoxaflor (sulfilimine; formulated as Gondola). We tested two ant (Hymenoptera: Formicidae) species with different colony founding strategies, Lasius niger (Linnaeus, 1758) and Myrmica rubra (Linnaeus, 1758). We sprayed their queens with insecticides at concentrations recommended for use in foliar applications in agriculture, i.e., at 1.25 g L-1 (acetamiprid), 0.6 g L-1 (sulfoxaflor), and 0.875 g L-1 (deltamethrin). Further, we diluted the compounds in distilled water and tested them at 10%, 1%, and 0.1% of the field-recommended concentrations, and used distilled water as a control. We monitored the survival of the queens and the number of eggs laid. All three tested insecticides caused severe lethal and sublethal concentration-dependent effects. Even at concentrations three orders of magnitudes lower than recommended for field applications, significantly lower numbers of eggs were found in the queens' nests. The extent of the sublethal effects of acetamiprid and sulfoxaflor was concentration-dependent and differed between the two ant species. Besides bees and bumblebees, ants represent an important group of hymenopterans that are severely affected even by low concentrations of the tested compounds and therefore should be included in risk assessment schemes.

Zobrazit více v PubMed

Thompson HM, Maus C. The relevance of sublethal effects in honey bee testing for pesticide risk assessment. Pest Manag. Sci. 2007;63:1058–1061. PubMed

Rose RI. Tier-based testing for effects of proteinaceous insecticidal plant-incorporated protectants on non-target arthropods in the context of regulátory risk assessments. IOBC WPRS Bull. 2006;29:143–150.

Schläppi D, Stroeymeyt N, Neumann P. Unintentional effects of neonicotinoids in ants (Hymenoptera: Formicidae) Myrmecol. News. 2021;31:181–184.

Ricupero M, Desneux N, Zappalà L, Biondi A. Target and non-target impact of systemic insecticides on a polyphagous aphid pest and its parazitoid. Chemosphere. 2020;247:125728. PubMed

Gontijo PC, Neto DOA, Oliveira RL, Michaud JP, Carvalho GA. Non-target impacts of soybean insecticidal seed treatments on the life history and behavior of Podisus nigrispinus, a predator of fall armyworm. Chemosphere. 2018;191:342–349. PubMed

Main AR, Webb EB, Goyne KW, Mengel D. Neonicotinoid insecticides negatively affect performance measures of non-target terrestrial arthropods: A meta-analysis. Ecol. Appl. 2018;28:1232–1244. PubMed

Desneux N, Decourtye A, Delpuech J-M. The sublethal effects of pesticides on beneficial arthropods. Annu. Rev. Entomol. 2007;52:81–106. PubMed

Evans AN, Llanos JEM, Kunin WE, Evison SEF. Indirect effects of agricultural pesticide use on parasite prevalence in wild pollinators. Agric. Ecosyst. Environ. 2018;258:40–48.

Korenko S, Saska P, Kysilková K, Řezáč M, Heneberg P. Prey contaminated with neonicotinoids induces feeding deterrent behavior of a common farmland spider. Sci. Rep. 2019;9:15895. PubMed PMC

Stanley DA, Garratt MP, Wickens JB, Wickens VJ, Potts SG, Raine NE. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature. 2015;528:548–550. PubMed PMC

Chagnon M, Kreutzweiser D, Mitchell EA, Morrissey CA, Noome DA, Van der Sluijs JP. Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Env. Sci. Poll. Res. 2015;22:119–134. PubMed PMC

Del Toro I, Ribbons R, Pelini S. The little things that run the world revisited: A review of anti-mediated ecosystem services and disservices (Hymenoptera: Formicidae) Myrmecol. News. 2012;17:133–146.

Vandermeer J, Perfecto I, Ibarra-Núñez G, Philpott S, Garcia-Ballinas JA. Ants (Azteca sp.) as potential biological control agents in organic chade coffee production in Southern Chiapas, Mexico. Agrofor. Syst. 2002;56:271–276.

Chailleux A, Stirnemann A, Leyes J, Deletre E. Manipulating natural enemy behavior to improve biological control: Attractants and repellents of a weaver ant. Entomol. Gen. 2019;38:191–210.

Frizzo TL, Souza LM, Sujii ER, Togni PH. Ants provide biological control on tropical organic farms influenced by local and landscape factors. Biol. Control. 2020;151:104378.

Hölldobler B, Wilson EO. The Ants. Springer; 1990.

Frouz J, Jílková V. The effect of ants on soil properties and processes (Hymenoptera: Formicidae) Myrmecol. News. 2008;11:191–199.

Schläppi D, et al. Varying impact of neonicotinoid insecticide and acute bee paralysis virus across castes and colonies of black garden ants, Lasius niger (Hymenoptera: Formicidae) Sci. Rep. 2021;11:20500. PubMed PMC

Song Y, et al. Research progress on bouncing behaviour and control technology of pesticide droplets at plant leaf surface. Chin. J. Pesticide Sci. 2019;21:895–907.

Sluijs, J. van der P. et al. Neonicotinoids, bee disorders and the sustainability of pollinator services. Curr. Opin. Environ. Sust.5, 293–305 (2013).

Seifert B. The Ants of Central and North Europe. Lutra Verlags- und Vertriebsgesellschaft; 2018.

Simon-Delso N, et al. Systemic insecticides (neonicotinoids and fipronil): Trends, uses, mode of action and metabolites. Env. Sci. Poll. Res. 2015;22:5–34. PubMed PMC

Epstein Y, Chapron G, Verheggen F. EU Court to rule on banned pesticide use. Science. 2021;373:290. PubMed

Jactel H, et al. Alternatives to neonicotinoids. Environ. Int. 2019;129:423–429. PubMed

Azpiazu C, et al. Toxicity of the insecticide sulfoxaflor alone and in the combination with the fungicide fluxapyroxad in three bee species. Sci. Rep. 2021;11:6821. PubMed PMC

Naharashi T, Frey JM, Ginsburg KS, Roy ML. Sodium and GABA-activated channels as the targets of pyrethroids and cyclodienes. Toxicol. Lett. 1992;64–65:429–436. PubMed

Davies TGE, Field LM, Usherwood PNR, Williamson MS. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life. 2007;59:151–162. PubMed

Desneux N, et al. Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J. Econ. Entomol. 2005;98:9–17. PubMed

Longhurst C, et al. Cross-resistance relationships of the sulfoximine insecticide sulfoxaflor with neonicotinoids and other insecticides in the whiteflies Bemisia tabaci and Trialeurodes vaporariorum. Pest Manag. Sci. 2013;69:809–813. PubMed

Siviter H, Brown MJF, Leadbeater E. Sulfoxaflor exposure reduces bumblebee reproductive success. Nature. 2018;561:109–112. PubMed

Siviter H, Homer J, Brown MJF, Leadbeater E. Sulfoxaflor exposure reduces egg laying in bumblebees Bombus terrestris. J. Appl. Ecol. 2020;57:160–169. PubMed PMC

Siviter H, Muth F. Do novel insecticides pose a threat to beneficial insects? Proc. R. Soc. B. 2020;287:20201265. PubMed PMC

Siviter H, et al. No evidence for negative impacts of acute sulfoxaflor exposure on bee olfactory conditioning or working memory. PeerJ. 2019;12:e7208. PubMed PMC

Pan F, Lu Y, Wang L. Toxicity and sublethal effects of sulfoxaflor on the red imported fire ant, Solenopsis invicta. Ecotoxicol. Environ. Saf. 2017;139:377–383. PubMed

Frankel TE, Frankel JS. Sulfoxaflor causes mortality, decreased locomotion, and altered interactions in pavement ants (Tetramorium caespitum) J. Environ. Sci. Health B. 2021;56:891–898. PubMed

Erickson BE. EPA to reconsider sulfoxaflor`s risk. C&EN. 2023;101:13.

Trompiz, G. French court suspends two Dow pesticides over potential harm to bees. Reuters, 24-Nov-2017. https://www.reuters.com/article/us-france-pesticides-idUSKBN1DO1M9 Accessed 12 July 2023.

Gill P, et al. Assessment of neonicotinoid insecticide adetamiprid LC50 against earthworm (Eisenia fetida L.) Environ. Ecol. 2021;39:1150–1153.

Song Y, Kai J, Song X, Zhang W, Li L. Long-term effects of deltamethrin and fenvalerante in soil. J. Hazard. Mat. 2015;289:158–164. PubMed

Fang S, et al. Lethal toxicity and sublethal metabolic interference effects of sulfoxaflor on the earthworm (Eisenia fetida) J. Agric. Food Chem. 2018;66:11902–11908. PubMed

Potts J, Cross P, MacDonald A, Jones D. Acetamiprid transport and mobility within UK agricultural soils—A comparison of commercial mixtures under different soil organic matter treatments. Geophys. Res. Abstr. 2019;21:EGU2019–19050.

Zhang L, Khan SU, Akhtar MH, Ivarson KC. Persistence, degradation, and distribution of deltamethrin in an organic soil under laboratory conditions. J. Agric. Food Chem. 1984;32:1207–1211.

Vig K, Singh DK, Agarwal HC, Dhawan AK, Dureja P. Insecticide residues in cotton crop soil. J. Environ. Sci. Health B. 2001;36:421–434. PubMed

USEPA/OPPTS. Pesticide Fact Sheet: Sulfoxaflor. EPA, Washington, DC. https://www.epa.gov/pesticides/factsheets/index.htm (2013).

NCBI. PubChem Compound Summary for CID 16723172, Sulfoxaflor. NCBI, Bethesda. https://pubchem.ncbi.nlm.nih.gov/compound/Sulfoxaflor (2022).

Peck SL, McQuaid B, Campbell CL. Using ant species (Hymenoptera: Formicidae) as a biological indicator of agroecosystem condition. Environ. Entomol. 1998;27:1102–1110.

Rodríguez, E., Peña, A., Raya, A. J. S., Campos, M. (2003). Evaluation of the effect on arthropod populations by using deltamethrin to control Phloeotribus scarabaeoides Bern. (Coleoptera: Scolytidae) in olive orchards. Chemosphere52, 127–134. PubMed

Wetterer JK, Radchenko AG. Worldwide spread of the ruby ant, Myrmica rubra (Hymenoptera: Formicidae) Myrmecol. News. 2011;14:87–96.

Schär S, et al. Do Holarctic ant species exist? Trans-Beringian dispersal and homoplasy in the Formicidae. J. Biogeogr. 2018;45:1917–1928.

Schär S, et al. Integrative taxonomy reveals cryptic diversity in North American Lasius ants, and an overlooked introduced species. Sci. Rep. 2022;12:5970. PubMed PMC

Rasse P, Deneubourg JL. Dynamics of nest excavation and nest size regulation of Lasius niger (Hymenoptera: Formicidae) J. Insect Behav. 2001;14:433–449.

Radchenko AG, Elmes GW. Myrmica ants of the old world. Fauna Mundi. 2010;3:1–789.

Anonymus. MOSPILAN 20 SP. https://www.agromanual.cz/download/pdf_etiketa/e_mospilan_20_sp.pdf (2021).

Gupta S, Gajbhiye VT. Persistence of acetamiprid in soil. Bull. Environ. Toxicol. 2007;78:349–352. PubMed

Anonymus. Sanium Ultra. https://www.prohopo.cz/userfiles/files/1240047_P%C5%99%C3%ADbalov%C3%BD%20let%C3%A1k%20(SBM%20Life%20Science)%20Sanium%20Ultra.pdf (2022).

Selim H, Zhu H. Retention and mobility of deltamethrin in soils: 2. Transport 1. Soil Sci. 2002;167:580–589.

Anonymus. Gondola. https://www.agrofert.cz/sites/default/files/downloads/gondola_0.pdf (2022).

Finney DJ. Probit analysis. J. Pharm. Sci. 1971;60:1432.

Dickinson JL, Hatchwell B. Fitness consequences of helping. In: Koenig WD, Dickinson JL, editors. Ecology and Evolution of Cooperative Breeding in Birds. Cambridge University Press; 2004. pp. 48–66.

Bernasconi G, Strassmann JE. Cooperation among unrelated individuals: The ant foundress case. Trends Ecol. Evol. 1999;14:477–482. PubMed

Lopez-Vaamonde C, et al. Lifetime reproductive success and longevity of queens in an annual social insect. J. Evol. Biol. 2009;22:983–996. PubMed

Keller L. The assessment of reproductive success of queens in ants and other social insects. Oikos. 1993;67:177–180.

Gammans N, Bullock JM, Schönrogge K. Ant benefits in a seed dispersal mutualism. Plant Anim. Interact. 2005;146:43–49. PubMed

Gibson RL, Scott JG. Comparative toxicity of fourteen insecticides to two species of carpenter ants (Hymenoptera:Formicidae) J. Econ. Entomol. 1989;82:1121–1124.

Barbieri RF, Lester PJ, Miller AS, Ryan KG. A neurotoxic pesticide changes the outcome of aggressive interactions between native and invasive ants. Proc. R. Soc. B. 2013;280:20132157. PubMed PMC

Heneberg P, Svoboda J, Pech P. Claustral colony founding does not prevent sensitivity to the detrimental effects of azole fungicides on the fecundity of ants. J. Environ. Manag. 2021;280:111740. PubMed

Rust MK, Reierson DA, Klotz JH. Delayed toxicity as a critical factor in the efficacy of aqueous baits for controlling Argentine ants (Hymenoptera: Formicidae) J. Econ. Entomol. 2004;97:1017–1024. PubMed

Wang L, Zeng L, Chen J. Impact of imidacloprid on new queens of imported fire ants, Solenopsis invicta (Hymenoptera: Formicidae) Sci. Rep. 2015;5:17938. PubMed PMC

Thiel S, Köhler H-R. A sublethal imidacloprid concentration alters foraging and competition behaviour of ants. Ecotoxicology. 2016;25:814–823. PubMed

Jung J-K, Jung C, Koh S-H. Lethal and sublethal effects of thiacloprid on non-target carpenter ant, Camponotus japonicas Mayr (Hymenoptera: Formicidae) J. Asia-Pac. Entomol. 2018;21:1321–1325.

Schläppi D, Kettler N, Straub L, Glauser G, Neumann P. Long-term effects of neonicotinoid insecticides on ants. Commun. Biol. 2020;3:335. PubMed PMC

Mokkapati JS, Bednarska AJ, Laskowski R. The development of the solitary bee Osmia bicornis is affected by some insecticide agrochemicals at environmentally relevant concentrations. Sci. Total Environ. 2021;775:145588. PubMed

Jurewicz J, et al. Exposure to pyrethroid pesticides and ovarian reserve. Environ. Int. 2020;144:106028. PubMed

Soeprono AM, Rust MK. Effect of delayed toxicity of chemical barriers to control Argentine ants (Hymenoptera: Formicidae) J. Econ. Entomol. 2004;97:2021–2028. PubMed

Sakamoto H, Goka K. Acute toxicity of typical ant control agents to the red imported fire ant, Solenopsis invicta (Hymenoptera: Formicidae) Appl. Entomol. Zool. 2021;56:217–224. PubMed PMC

Müller T, Gesing MA, Segeler M, Müller C. Sublethal insecticide exposure of an herbivore alters the response of its predator. Environ. Pollut. 2019;247:39–45. PubMed

Dai PL, et al. Effects of sublethal concentrations of bifenthrin and deltamethrin on fecundity, growth, and development of the honeybee Apis mellifera ligustica. Environ. Toxicol. Chem. 2010;29:644–649. PubMed

Teder T, Knapp M. Sublethal effects enhance detrimental impact of insecticides on non-target organisms: A quantitative synthesis in parasitoids. Chemosphere. 2019;214:371–378. PubMed

Yang Y, et al. Acute and chronic toxicity of acetamiprid, carbaryl, cypermethrin and deltamethrin to Apis mellifera larvae reared in vitro. Pest Manag. Sci. 2020;76:978–985. PubMed

Reissert-Oppermann S, Bauer B, Steuber S, Clausen PH. Insecticide resistence in stable flies (Stomoxys calcitrans) on dairy farms in Germany. Parasitol. Res. 2019;118:2499–2507. PubMed

Babcock JM, et al. Biological characterization of sulfoxaflor, a novel insecticide. Pest Manag. Sci. 2011;67:328–334. PubMed

Directorate-General for Health and Food Safety. Sulfoxaflor: Commission restricts the use of harmful pesticide for pollinators. https://food.ec.europa.eu/news/sulfoxaflor-commission-restricts-use-harmful-pesticide-pollinators-2022-04-07_en Accessed 3 August 2023.

EFSA, et al. Peer review of the pesticide risk assessment for the active substance sulfoxaflor in light of confirmatory data submitted. EFSA J.17, 5633 (2019). PubMed PMC

EPA. Addendum to the environmental fate and ecological risk assessment for sulfoxaflor registration. (Environmental Protection Agency, Washington, 2016)

EPA. Decision memorandum supporting the registration decision for new uses of the active ingredient sulfoxaflor on alfalfa, cacao, citrus, corn, cotton, cucurbits, grains, pineapple, sorghum, soybeans, strawberries and tree plantations. (Environmental Protection Agency, Washington, 2019)

Li J, et al. Sublethal effects of Isoclast™ Active (50% sulfoxaflor water dispersible granules) on larval and adult worker honey bees (Apis mellifera L.) Ecotoxicol. Environ. Saf. 2021;220:112379. PubMed

Sanders D, van Veen FJF. Ecosystem engineering and predation: The multi-trophic impact of two ant species. J. Anim. Ecol. 2011;80:569–576. PubMed

Fiedler K. Ant-associates of Palaearctic lycaenid butterfly larvae (Hymenoptera: Formicidae; Lepidoptera: Lycaenidae)—A review. Myrmecol. News. 2006;9:77–87.

Petal J. Ant populations, their regulation and effect on soil in meadows. Ekol. Pol. 1980;28:297–326.

Petal J, Kusinska A. Fractional composition of organic matter in the soil of anthills and of the environment of meadows. Pedobiol. 1994;38:493–501.

Servigne P, Detrain C. Ant-seed interactions: Combined effects of ant and plant species on seed removal patterns. Insectes Soc. 2008;55:220–230.

Fiedler K, Kuhlmann F, Schlick-Steiner BC, Steiner FM, Gebauer G. Stable N-isotope signatures of central European ants—Assessing positions in a trophic gradient. Insectes Soc. 2007;54:393–402.

Keller L, Passera L. Size and fat content of gynes in relation to the mode of colony founding in ants (Hymenoptera: Formicidae) Oecologia. 1989;80:236–240. PubMed

Lamichhane JR. Thirteen decades of antimicrobial copper compounds applied in agriculture. A review. Agron. Sustain. Dev. 2018;38:28.

EFSA Ppr Panel Scientific opinion addressing the state of the science on risk assessment of plant protection products for in-soil organisms. EFSA J. 2017;15:4690. PubMed PMC

OECD. OECD Guidelines for the Testing of Chemicals, Section 2 - Effects on Biotic Systems. 10.1787/20745761 (2019).

Fojtová D, et al. Nanoformulations can significantly affect pesticide degradation and uptake by earthworms and plants. Environ. Chem. 2019;16:470–481.

Xu Z, et al. Environmental risks and the potential benefits of nanopesticides: A review. Environ. Chem. Lett. 2022;20:2097–2108.

Padmavathi P, Vasundhara N, Kovvuri S, Venugopal N. Synthesis and characterization of nano-acetamiprid-new plant safeguard material. Am. J. Anal. Chem. 2020;11:197–204.

Ebadollahi A, et al. Nanoencapsulation of acetamiprid by sodium alginate and polyethylene glycol enhanced its insecticidal efficiency. Nanomaterials. 2022;12:2971. PubMed PMC

Khalifa AG, et al. Deltamethrin and its nanoformulations induce behavioral alteration and toxicity in rat brain through oxidative stress and JAK2/STAT3 signaling pathway. Toxics. 2022;10:303. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...