, Volume 62, Issue 2, pp 197–208 | Cite as

Compatibility of sulfoxaflor and other modern pesticides with adults of the predatory mite Amblyseius swirskii. Residual contact and persistence studies

  • M. Mar FernándezEmail author
  • Pilar Medina
  • Andrea Wanumen
  • Pedro Del Estal
  • Guy Smagghe
  • Elisa Viñuela


Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) is a very efficient generalist predatory mite of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) and Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), worldwide released in horticultural greenhouses. Here, the toxicity of sulfoxaflor and other ten pesticides to A. swirskii adults when applied at their maximum field rate was assessed in the laboratory in terms of mortality and reproductive performance. The duration of the harmful activity when residues were aged under greenhouse was assessed for compounds not classified as harmless in the laboratory, based on the International Organization for Biological Control (IOBC) rules. Sulfoxaflor as well as flonicamid, flubendiamide, metaflumizone, methoxyfenozide, spiromesifen, and spirotetramat were harmless, emamectin was slightly harmful and abamectin, deltamethrin and spinosad were harmful. Emamectin was short-lived and abamectin, deltamethrin and spinosad were slightly persistent under our conditions.


Amblyseius swirskii Side effects Natural enemy IOBC Horticultural crops Greenhouse 



This study was supported by the Spanish Ministry of Science and Innovation (Projects AGL2010-22196-C02-02 and AGL2013-47603-C2-1-R to E. Viñuela and P. Medina and PhD grant to Mª M. Fernández). E. Viñuela, P. del Estal and P. Medina are members of the Associate Unit IVAS (CSIC-UPM): Control of insect vectors of viruses in horticultural sustainable systems.


  1. Amor F, Medina P, Bengochea P, Cánovas M, Vega P, Correia R, García F, Gómez M, Budia F, Viñuela E, López J (2012) Effect of emamectin benzoate under semi-field and field conditions on key predatory biological control agents used in vegetable greenhouse. Biocontrol Sci Technol 22(2):219–232CrossRefGoogle Scholar
  2. Babcock JM, Gerwick CB, Huang JX, Loso MR, Nakamura G, Nolting SP, Rogers RB, Sparks TC, Thomas J, Whatson GB, Zhu Y (2011) Biological characterization of sulfoxaflor, a novel insecticide. Pest Manag Sci 67(3):328–334CrossRefPubMedGoogle Scholar
  3. Barrett KI, Grandy N, Harrison EG, Hassan SA, Oomen P (1994) Guidance document on regulatory testing procedures for pesticides with non-target arthropods. SETAC, BelgiumGoogle Scholar
  4. Beers EH, Schmidt RA (2014) Impacts of orchard pesticides on Galendromus occidentalis: lethal and sublethal effects. Crop Prot 56:16–24CrossRefGoogle Scholar
  5. Bengochea P, Sánchez-Ramos I, Saelices R, Amor F, del Estal P, Viñuela E, Adán A, López A, Budia F, Medina P (2014) Is emamectin benzoate effective against the different stages of Spodoptera exigua (Hübner) (Lepidoptera, Noctuidae)? Irish J Agric Food Res 53:37–49Google Scholar
  6. Bernard MB, Cole P, Kobelt A, Horne PA, Altmann J, Wratten SD, Yen AL (2010) Reducing the impact of pesticides on biological control in australian vineyards: pesticide mortality and fecundity effects on an indicator species, the predatory mite Euseius victoriensis (Acari: Phytoseiidae). J Econ Entomol 103(6):2061–2071CrossRefPubMedGoogle Scholar
  7. Bielza P (2008) Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis. Pest Manag Sci 64:1131–1138CrossRefPubMedGoogle Scholar
  8. Biondi A, Desneux N, Siscaro G, Zappalà L (2012a) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87(7):803–812CrossRefPubMedGoogle Scholar
  9. Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalà L, Desneux N (2012b) Non-target impact of spinosyns on beneficial arthropods, a review. Pest Manag Sci 68(12):1523–1536CrossRefPubMedGoogle Scholar
  10. Blümel S, Hausdorf H (2002) Results of the 8th and 9th IOBC Joint Pesticides Testing Programme: persistence test with Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae). IOBC/WPRS Bull 25(11):43–51Google Scholar
  11. Bonafos R, Serrano E, Auger P, Kreiter S (2007) Resistance to deltamethrin, lambda-cyhalothrin and chlorpyriphos-ethyl in some populations of Typhlodromus pyri Scheuten and Amblyseius andersoni (Chant) (Acari: Phytoseiidae) from vineyards in the south-west of France. Crop Prot 26:169–172CrossRefGoogle Scholar
  12. Bostanian NJ, Akalach M (2006) The effect of indoxacarb and five other insecticides on Phytoseiulus persimilis (Acari: Phytodeiidae), Amblyseius fallacis (Acari: Phytoseiidae) and nymphs of Orius insidiosus (Hemiptera: Anthocoridae). Pest Manag Sci 62:334–339CrossRefPubMedGoogle Scholar
  13. Bostanian NJ, Hardman JM, Thistlewood HA, Racette G (2010) The response of Neoseiulus fallacies (Garman) and Galendromus occidentalis (Nesbitt) (Acari: Phytoseiidae) to six reduced risk insecticides in Canada. IOBC/WPRS Bull 55:73–77Google Scholar
  14. Broufas GD, Pappas ML, Vassiliou G, Koveos DS (2008) Toxicity of certain pesticides to the predatory mite Euseius finlandicus (Acari: Phytoseiidae). IOBC/WPRS Bull 35:85–91Google Scholar
  15. Calvo FJ, Bolckmans K, Belda JE (2011) Control of Bemisia tabaci and Frankliniella occidentalis in cucumber by Amblyseius swirskii. BioControl 56(2):185–192CrossRefGoogle Scholar
  16. Carlson GR, Dhadialla TS, Hunter R, Jansson RK, Jany CS, Lidert Z, Slawecki RA (2001) The chemical and biological properties of methoxyfenozide, a new insecticidal ecdysteroid agonist. Pest Manag Sci 57:115–119CrossRefPubMedGoogle Scholar
  17. Cheon GS, Paik CH, Kim SS (2008) Selective toxicity of three acaricides to the predatory mite Neoseiulus womersleyi and its prey Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae). Korean J Pestic Sci 12:249–255Google Scholar
  18. Cloyd RA, Galle CL, Keith S (2006) Compatibility of three miticides with the predatory mites Neoseiulus californicus McGregor and Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae). HortScience 41(3):707–710Google Scholar
  19. Colomer I, Aguado P, Medina P, Heredia RM, Fereres A, Belda JE, Viñuela E (2011) Field trial measuring the compatibility of methoxyfenozide and flonicamid with Orius laevigatus Fieber (Hemiptera: Anthocoridae) and Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) in comercial pepper greenhouse. Pest Manag Sci 67:1237–1244CrossRefPubMedGoogle Scholar
  20. De Barro PJ, Liu SS, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19CrossRefPubMedGoogle Scholar
  21. De Cabezón Sáenz, Irigaray FJ, Zalom FG (2007) Selectivity of acaricide exposure on Galendromus occidentalis reproductive potential. Biocontrol Sci Techn 17(5):541–546CrossRefGoogle Scholar
  22. Desneux N, Decourteye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106CrossRefPubMedGoogle Scholar
  23. Doker I, Pappas ML, Samaras C, Triantafyllou A, Kazak C, Broufas GD (2015) Compatibility of reduced-risk insecticides withy the non-target predatory mite Iphiseius degenerans (Acari: Phytoseiidae). Pest Manag Sci 71(9):1267–1273CrossRefPubMedGoogle Scholar
  24. EPA (Environmental Protection Agency) (2008) EPA spirotetramat fact sheet. Cited 9 March 2016
  25. EPA (Environmental Protection Agency) (2013) Pesticide news story: The EPA’s final decision on the new active ingredient sulfoxaflor. Cited 21 March 2016
  26. EPPO (European and Mediterranean Plant Protection Organization) (2015a) Data sheets on quarantine pests: Bemisia tabaci. Cited 9 March 2016
  27. EPPO (European and Mediterranean Plant Protection Organization) (2015b) Data sheets on quarantine pests: Frankliniella occidentalis. Cited 9 March 2016
  28. Fernández E, Grávalos C, Haro PJ, Cifuentes D, Bielza P (2009) Insecticide resistance status of Bemisa tabaci Q-biotype in south-eastern Spain. Pest Manag Sci 65:885–891CrossRefPubMedGoogle Scholar
  29. Garzón A, Medina P, Amor F, Viñuela E, Budia F (2015) Toxicity and sublethal effects of six insecticides to last instar larvae and adults of the biocontrol agents Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and Adalia bipunctata (L.) (Coleoptera: Coccinellidae). Chemosphere 132:87–93CrossRefPubMedGoogle Scholar
  30. Gentz MC, Murdoch G, King GF (2010) Tandem use of selective insecticides and natural enemies for effective reduced-risk pest management. Biol Control 52(3):208–215CrossRefGoogle Scholar
  31. Gómez M, Garcia F, GreatRex R, Lorca M, Serna A (2006) Preliminary field trials with the synthetic sexual aggregation pheromone of Frankliniella occidentalis on protected pepper and tomato crops in south-east Spain. IOBC/WPRS Bull 29(4):153–158Google Scholar
  32. Gradish AE, Scott-Dupree CD, Shipp L, Harris CR, Ferguson G (2011) Effect of reduced risk pesticides on greenhouse vegetable arthropod biological control agents. Pest Manag Sci 67:82–86CrossRefPubMedGoogle Scholar
  33. Hassan SA (1994) Activities of the IOBC/WPRS working group Pesticides and Beneficial Organisms. IOBC/WPRS Bull 17:1–5Google Scholar
  34. IOBC (International Organization for Biological Control) (2016) IOBC Pesticide Side Effect Database. Cited 3 March 2016
  35. IRAC (Insecticide Resistance Action Committee) (2016) Mode of action classification scheme (version 8.0). Cited 10 Feb 2016
  36. Jacas J, Viñuela E (1994) Analysis of a laboratory method to test the effects of pesticides on adult females of Opius concolor (Hymn.: Braconidae), a parasitoid of the olive fruit fly Bactrocera oleae (Dip.: Tephritidae). Biocontrol Sci Technol 4:147–154CrossRefGoogle Scholar
  37. Jansen JP (2010) Beneficial arthropods and pesticides: building selectivity lists for IPM. IOBC/WPRS Bull 55:23–47Google Scholar
  38. Kim SS, Seo SG, Park JD, Kim SG, Kim DI (2005) Effects of selected pesticides on the predatory mite, Amblyseius cucumeris (Acari: Phytoseiidae). J Entomol Sci 40(2):107–114Google Scholar
  39. Lefebvre M, Bostanian NJ, Thistlewood HMA, Mauffette Y, Racette G (2011) A laboratory assessment of the toxic attributes of six ‘reduced risk insecticides’ on Galendromus occidentalis (Acari: Phytoseiidae). Chemosphere 84:25–30CrossRefPubMedGoogle Scholar
  40. Lefebvre M, Bostanian NJ, Mauffette Y, Racette G, Thistlewood HA, Hardman JM (2012) Laboratory-based toxicological assessments of new insecticides on mortality and fecundity of Neoseiulus fallacis (Acari: Phytoseiidae). J Econ Entomol 105(3):866–871CrossRefPubMedGoogle Scholar
  41. Liu P, Liu Y, Liu Q, Liu J (2010) Photodegradation mechanism of deltamethrin and fenvalerate. J Environ Sci 22(7):1123–1128CrossRefGoogle Scholar
  42. MAGRAMA (Ministry of Agriculture, Food and environment) (2016a) Annual survey directory 2012. Madrid. Cited 22 Feb 2016 (in Spanish)
  43. MAGRAMA (Ministry of Agriculture, Food and environment) (2016b) European community list of active substances included, excluded and under evaluation. Cited 10 Feb 2016 (in Spanish)
  44. MAGRAMA (Ministry of Agriculture, Food and environment) (2016c) Official phytosanitary products entry. Cited 10 Feb 2016 (in Spanish)
  45. Nadimi A, Kamali K, Arbabi M, Abdoli F (2011) Study on persistence tests of miticides abamectin and fenproximate to predatory mite Phytoseiulus persimilis (Acarina: Phytoseiidae). Afr J Agric Res 6(2):338–342Google Scholar
  46. OJEC (Official Journal of the European Community) (2008) Commision regulation (EC) No. 404/2008 of 6 May 2208 amending Annex II to Council Regulation (EEC) No. 2092/91 on organic production of agricultural products as concerns the authorization of spinosad, potassium bicarbonate and copper octanoate and the use of ethylene. OJEC 120:8–10Google Scholar
  47. OJEU (Official Journal of the European Union) (2009) Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2009, establishing a framework for Community action to achieve the sustainable use of pesticides. OJEU 309:71–86Google Scholar
  48. Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723CrossRefGoogle Scholar
  49. Rahman T, Spafforda H, Broughton S (2011) Compatibility of spinosad with predaceous mites (Acari) used to control Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Pest Manag Sci 67:993–1003CrossRefPubMedGoogle Scholar
  50. Robledo Camacho A, van der Blom J, Sánchez Martínez JA, Torres Giménez S (2009) Control biológico en invernaderos hortícolas. Coexphal-FAECA, Almería (in Spanish)Google Scholar
  51. Roditakis E, Fytrou N, Staurakaki M, Vontas J, Tsagkarakou A (2014) Activity of flonicamid on the sweet potato whitely Bemisia tabaci (Homoptera: Aleyrodidae) and its natural enemies. Pest Manag Sci 70:1460–1467CrossRefPubMedGoogle Scholar
  52. Rodrigues JR, Miranda NRC, Rosas JDF, Maciel CM, Torres LM (2002) Side-effects of fifteen insecticides on predatory mites (Acari: Phytoseiidae) in apple orchards. IOBC/WPRS Bull 25(11):53–61Google Scholar
  53. Roubos CR, Rodriguez-Saona C, Rufus I (2014) Mitigating the effects of insecticides on arthropod biological control at field and landscape scales. Biol Control 75:28–38CrossRefGoogle Scholar
  54. Shipp JL, Wang K, Binns MR (2000) Economic injury levels for western flower thrips (Thysanoptera: Thripidae) on greenhouse cucumber. J Econ Entomol 93(6):1732–1740CrossRefPubMedGoogle Scholar
  55. Smagghe G, Gomez LE, Dhadialla TS (2013) The bisacylhydrazine insecticides for selective pest control. Adv Insect Physiol 43:163–249CrossRefGoogle Scholar
  56. Sparks T, Watson G, Loso M, Geng C, Babcock J, Thomas J (2013) Sulfoxaflor and the sulfoximine insecticides: chemistry, mode of action and basis for efficacy on resistant insects. Pestic Biochem Physiol 107:1–7CrossRefPubMedGoogle Scholar
  57. Sterk G, Heuts F, Merck N, Bock J (2003) Sensitivity of non-target arthropods and beneficial fungal species to chemical and biological plant protection products: results of laboratory and semi-field trials. In: Proceedings of the first international symposium on biological control of arthropods, USDA forest service, Honolulu, USA, pp 306–313Google Scholar
  58. STSC (1987) Statgraphics user’s guide, Version 5.1. Graphic software system. STSC, Rockville, USAGoogle Scholar
  59. Tirello P, Pozzebon A, Duso C (2013) The effect of insecticides on the non-target predatory mite Kampimodromus aberrans: laboratory studies. Chemosphere 93:1139–1144CrossRefPubMedGoogle Scholar
  60. Tohnishi M, Nakao H, Furuya T, Seo A, Kodama H, Tsubata K, Fujioka S, Kodama H, Hirooka T, Nishimatsu T (2005) Flubendiamide, a novel insecticide highly active against lepidopterous insect pests. J Pestic Sci 30(4):354–360CrossRefGoogle Scholar
  61. van de Veire M, Tirry L (2003) Side effects of pesticides on four species of beneficials used in IPM in glasshouse vegetable crops: “worst case” laboratory tests. IOBC/WPRS Bull 26(5):41–50Google Scholar
  62. van de Veire M, Cornelis W, Tirry L (2001) Development of a laboratory test method to determine the duration of pesticide-effects on predatory mites. IOBC/WPRS Bull 24(4):61–66Google Scholar
  63. van de Veire M, Viñuela E, Bernardo U, Tirry L, Adan A, Viggiani G (2004) Duration of the toxicity of abamectin and spinosad on the parasitic wasp Encarsia formosa Gahan in Northern and Southern Europe. IOBC/WPRS Bull 27(6):21–30Google Scholar
  64. Wanumen AC, Carvalho GA, Medina P, Viñuela E, Adán A (2016) Residual acute toxicity of some modern insecticides toward two mirid predators of tomato pests. J Econ Entomol 109(3):1079–1085CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2017

Authors and Affiliations

  • M. Mar Fernández
    • 1
    Email author
  • Pilar Medina
    • 1
  • Andrea Wanumen
    • 1
  • Pedro Del Estal
    • 1
  • Guy Smagghe
    • 2
  • Elisa Viñuela
    • 1
  1. 1.Crop Protection Unit, School of Agricultural SciencesTechnical University of Madrid (UPM)MadridSpain
  2. 2.Department of Crop Protection, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium

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