Improved control of Frankliniella occidentalis on greenhouse pepper through the integration of Orius sauteri and neonicotinoid insecticides

Abstract

Frankliniella occidentalis (Thysanoptera: Thripidae) is a notorious pest of horticultural crops, against which the predator Orius sauteri or neonicotinoid insecticides are commonly used in control programmes. Here, we carried out a series of indoor acute toxicity tests and a risk assessment of eight neonicotinoid insecticides (imidacloprid, nitenpyram, acetamiprid, thiacloprid, thiamethoxam, clothianidin, dinotefuran and flupyradifurone) for O. sauteri and F. occidentalis. For O. sauteri, the LC50 values of acetamiprid and flupyradifurone were 12.75 and 9.24 mg a.i. L−1, respectively, and their hazard quotients were ≤ 2. Their toxicities to F. occidentalis were in a similar range. When LC20 of acetamiprid or flupyradifurone was applied to the pest, predator or both, predation ability was slightly reduced with flupyradifurone (37, 59 and 18, respectively) having less impact compared to acetamiprid (18, 21 and 10, respectively). Furthermore, we performed a greenhouse efficacy trial which involved the selected neonicotinoids acetamiprid and flupyradifurone as well as O. sauteri. Our results showed that integrated pest management, i.e. the application of half the amount of O. sauteri together with low doses (LC20) of acetamiprid or flupyradifurone, significantly reduced the pest with 76% and 75%, respectively, during the trial time, similar to the biocontrol treatment and significantly better than for chemical control alone. The cost of the integrated pest control strategy was similar to chemical control alone and lower than for biocontrol, indicating its potential as an economically feasible thrips control strategy, with reduced environmental risks compared to using chemicals only.

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References

  1. Bass C, Denholm I, Williamson MS, Nauen R (2015) The global status of insect resistance to neonicotinoid insecticides. Pestic Biochem Phys 121:78–87

    CAS  Google Scholar 

  2. Bielza P (2008) Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis. Pest Manag Sci 64:1131–1138

    CAS  PubMed  Google Scholar 

  3. 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 Int 22:35–67

    CAS  PubMed  Google Scholar 

  4. Broughton S, Herron GA (2009) Potential new insecticides for the control of western flower thrips (Thysanoptera: Thripidae) on sweet pepper, tomato, and lettuce. J Econ Entomol 102:646–651

    CAS  PubMed  Google Scholar 

  5. Candolfi MP, Barrett KL, Campbell PJ, Forster R, Grandy N, Huet MC, Lewis G, Oomen PA, Schmuck R, Vogt H (2000) Guidance document on regulatory testing and risk assessment procedures for plant protection products with nontarget arthropods. ESCORT2 workshop

  6. Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Cloyd RA, Bethke JA (2011) Impact of neonicotinoid insecticides on natural enemies in greenhouse and interiorscape environments. Pest Manag Sci 67:3–9

    CAS  PubMed  Google Scholar 

  8. Demirozer O, Tyler-Julian K, Funderburk J, Leppla N, Reitz S (2012) Frankliniella occidentalis (Pergande) integrated pest management programs for fruiting vegetables in Florida. Pest Manag Sci 68:1537–1545

    CAS  PubMed  Google Scholar 

  9. European Commission (2018a) Commission Implementing Regulation (EU) 2018/783 of 29 May 2018 amending Implementing Regulation (EU) No 540/2011 as regards the conditions of approval of the active substance imidacloprid. Off J Eur Union 132:31–34

    Google Scholar 

  10. European Commission (2018b) Commission Implementing Regulation (EU) 2018/784 of 29 May 2018 amending Implementing Regulation (EU) No 540/2011 as regards the conditions of approval of the active substance clothianidin: L 132/35-39

  11. European Commission (2018c) Commission Implementing Regulation (EU) 2018/785 of 29 May 2018 amending Implementing Regulation (EU) No 540/2011 as regards the conditions of approval of the active substance thiamethoxam. Off J Eur Union 132:40–44

    Google Scholar 

  12. European Food Safety Authority (2011) Conclusion on the peer review of the pesticide risk assessment of the active substance acetochlor. EFSA J 9:2143

    Google Scholar 

  13. Gao YL, Lei ZR, Reitz SR (2012) Western flower thrips resistance to insecticides: detection, mechanisms and management strategies. Pest Manag Sci 68:1111–1121

    CAS  PubMed  Google Scholar 

  14. Gilbertson RL, Batuman O, Webster G, Adkins S (2015) Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annu Rev Virol 2:67–93

    CAS  PubMed  Google Scholar 

  15. Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987

    Google Scholar 

  16. He D, Lin RH, Men XY, Sun M, Cheng SH, Jiang H, Yu CH, Zheng L (2018) Ecological risk assessment of 16 pesticides to Orius sauteri. Asian J Ecotox 13:23–30

    Google Scholar 

  17. Hemerik L, Yano E (2011) Scaling up from individual behaviour of Orius sauteri foraging on Thrips palmi to its daily functional response. Popul Ecol 53:563–572

    Google Scholar 

  18. Hou ZR, Li J, Li JP, Sun BB, Yin Z, Wang JX, Guo XH (2018) Effectiveness of Orius sauteri (Poppius) for the control of thrips on greenhouse vegetables. Hubei Agric Sci 57:67–69

    Google Scholar 

  19. Jensen SE (2000) Insecticide resistance in the western flower thrips, Frankliniella occidentalis. Integr Pest Manag Rev 5:131–146

    Google Scholar 

  20. Kirk WDJ, Terry LI (2003) The spread of the western flower thrips Frankliniella occidentalis Pergande. Agric For Entomol 5:301–310

    Google Scholar 

  21. Li DG, Shang XY, Reitz S, Nauen R, Lei ZR, Lee SH, Gao YL (2016) Field resistance to spinosad in western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae). J Integr Agric 15:2803–2808

    CAS  Google Scholar 

  22. Lin RH, Yu CH, Jiang H, Yuan SK, Ma XD, Li WJ, Qu MM, Zhou YM, Zhou XX (2016) Guidance on environmental risk assessment for pesticide registration-Part 7: non-target arthropod. Standards Press of China

  23. Lu YB, Zhang ZJ, Wu QJ, Du YZ, Zhang HR, Yu Y, Wang ED, Wang MH, Wang MQ, Tong XL, Lu LH, Tan XQ, Fu WD (2011) Research progress of the monitoring, forecast and sustainable management of invasive alien pest Frankliniella occidentalis in China. Chin J Appl Entomol 48:488–496

    CAS  Google Scholar 

  24. Lv B, Sun M, Zhai YF, Chen H, Yu Y, Zheng L (2018) Effect of short adaptive pre-feeding on the predatory functional response to Orius sauteri reared on Sitotroga cerealella eggs. Chin J Environ Entomol 40:64–69

    Google Scholar 

  25. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573–580

    CAS  PubMed  Google Scholar 

  26. Morse JG, Hoddle MS (2006) Invasion biology of thrips. Annu Rev Entomol 1:67–89

    Google Scholar 

  27. Nagai K, Yano E (2000) Predation by Orius sauteri (Poppius) (Heteroptera: Anthocoridae) on Thrips palmi Karny (Thysanoptera: Thripidae). Functional response and selective predation. Appl Entomol Zool 35:565–574

    Google Scholar 

  28. Otieno JA, Pallmann P, Poehling HM (2017) Additive and synergistic interactions amongst Orius laevigatus (Heteroptera: Anthocoridae), entomopathogens and azadirachtin for controlling western flower thrips (Thysanoptera: Thripidae). Biocontrol 62:85–95

    CAS  Google Scholar 

  29. Prabhaker N, Castle SJ, Naranjo SE, Toscano NC, Morse JG (2011) Compatibility of two systemic neonicotinoids, imidacloprid and thiamethoxam, with various natural enemies of agricultural pests. J Econ Entomol 104:773–781

    CAS  PubMed  Google Scholar 

  30. Reitz SR (2009) Biology and ecology of the western flower thrips (Thysanoptera: Thripidae): the making of a pest. Fla Entomol 1:7–13

    Google Scholar 

  31. Roditakis E, Stavrakaki M, Grispou M, Achimastou A, Van Waetermeulen X, Nauen R, Tsagkarakou A (2017) Flupyradifurone effectively manages whitefly Bemisia tabaci MED (Hemiptera: Aleyrodidae) and tomato yellow leaf curl virus in tomato. Pest Manag Sci 73:1574–1584

    CAS  PubMed  Google Scholar 

  32. Saito T, Brownbridge M (2018) Compatibility of foliage-dwelling predatory mites and mycoinsecticides, and their combined efficacy against western flower thrips Frankliniella occidentalis. J Pest Sci 91:1291–1300

    Google Scholar 

  33. Tang Q, Ma K, Chi H, Hou Y, Gao X (2019) Transgenerational hormetic effects of sublethal dose of flupyradifurone on the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). PLoS ONE 14:e0208058

    CAS  PubMed  PubMed Central  Google Scholar 

  34. The Economic Times (2015) China targets zero growth in chemical fertilizer use in 2020, 18 Mar 2015. Xinhua News Agency, China

    Google Scholar 

  35. Utsumi T, Miyamoto M, Katagi T (2011) Ecotoxicological risk assessment of pesticides in terrestrial ecosystems. Environmental Health Science Laboratory, Sumitomo Chemical Co., Ltd.: Tokyo, Japan

  36. Vaello T, Casas JL, Pineda A, de Alfonso I, Marcos-García MÁ (2017) Olfactory response of the Predatory Bug Orius laevigatus (Hemiptera: Anthocoridae) to the aggregation pheromone of its prey, Frankliniella occidentalis (Thysanoptera: Thripidae). Environ Entomol 46:1115–1119

    PubMed  Google Scholar 

  37. Waite MO, Scott-Dupree CD, Brownbridge M, Buitenhuis R, Murphy G (2014) Evaluation of seven plant species/cultivars for their suitability as banker plants for Orius insidiosus (Say). Biocontrol 59:79–87

    CAS  Google Scholar 

  38. Wang S, Michaud JP, Tan XL, Zhang F (2014) Comparative suitability of aphids, thrips and mites as prey for the flower bug Orius sauteri (Hemiptera: Anthocoridae). Eur J Entomol 111:221–226

    Google Scholar 

  39. Wang ZH, Gong YJ, Jin GH, Jin GH, Li BY, Chen JC, Kang ZJ, Wei SJ (2016) Field-evolved resistance to insecticides in the invasive western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in China. Pest Manag Sci 72:1440–1444

    CAS  PubMed  Google Scholar 

  40. Wu SY, Gao YL, Xu XN, Goettel MS, Lei ZR (2015) Compatibility of Beauveria bassiana with Neoseiulus barkeri for control of Frankliniella occidentalis. J Integr Agric 14:98–105

    Google Scholar 

  41. Wu S, Zhang Z, Gao Y, Xu X, Lei Z (2016) Interactions between foliage-and soil-dwelling predatory mites and consequences for biological control of Frankliniella occidentalis. Biocontrol 61:717–727

    Google Scholar 

  42. Wu S, He Z, Wang E, Xu X, Lei Z (2017) Application of Beauveria bassiana and Neoseiulus barkeri for improved control of Frankliniella occidentalis in greenhouse cucumber. Crop Prot 96:83–87

    Google Scholar 

  43. Xu HH (2010) Phytochemical conservation. China Agricultural Press, Beijing

    Google Scholar 

  44. Zhang GF, Lu ZC, Wan FH, Lövei G (2007) Real-time PCR quantification of Bemisia tabaci (Homoptera: Aleyrodidae) B-biotype remains in predator guts. Mol Ecol Notes 7:947–954

    CAS  Google Scholar 

  45. Zhang ZJ, Zhang YJ, Xu BY, Zhu GR, Lv YB, Wu QJ (2013) Toxicity of different types of insecticides to Frankliniella occidentalis. J Zhejiang Agric Sci 6:694–697

    Google Scholar 

  46. Zhao J, Guo X, Tan X, Desneux N, Zappala L, Zhang F, Wang S (2017) Using Calendula officinalis as a floral resource to enhance aphid and thrips suppression by the flower bug Orius sauteri (Hemiptera: Anthocoridae). Pest Manag Sci 73:515–520

    CAS  PubMed  Google Scholar 

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Funding

This work was funded by the National Key R&D Program of China (2017YFD0201000, 2017YFGH000664), the Shandong Provincial Taishan Industry Leading Talents Project, China, the Shandong Provincial Major Science and Technology Innovation Project, China (2018CXGC0206), the Agricultural Science and Technology Innovation Project of Shandong Academy of Agricultural Sciences, China (CXGC2017B05) and the Shandong Provincial Modern Agricultural Industry Technology System Innovation Team Foundation, China (SDAIT-24-01).

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YFZ, QCL and HC designed the research. JPZ, FZ, XYD, ZWS, ZPS and GAW conducted experiments. HC, DB, XLD, YY and LZ analysed data. YFZ, QCL and DB wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Yi-fan Zhai.

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Special Issue on novel management tactics for the Western Flower Thrips.

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Lin, Qc., Chen, H., Babendreier, D. et al. Improved control of Frankliniella occidentalis on greenhouse pepper through the integration of Orius sauteri and neonicotinoid insecticides. J Pest Sci 94, 101–109 (2021). https://doi.org/10.1007/s10340-020-01198-7

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Keywords

  • Frankliniella occidentalis
  • Integrated pest management (IPM)
  • Neonicotinoid insecticides
  • Orius sauteri