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Additive and synergistic interactions amongst Orius laevigatus (Heteroptera: Anthocoridae), entomopathogens and azadirachtin for controlling western flower thrips (Thysanoptera: Thripidae)

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Abstract

This study evaluated the efficacy of the foliage-dwelling predator Orius laevigatus, soil applied entomopathogens and azadirachtin alone and in combinations for controlling western flower thrips (WFT). Evaluated products were Nemastar® Steinernema carpocapsae (E-nema) and O. laevigatus (Re-natur), Metarhizium anisopliae isolate ICIPE-69 and NeemAzal-T (azadirachtin) (Trifolio). Efficacy against WFT was significantly improved by combined treatments achieving 62–97 % reduction in WFT emergence, compared to 45–74 % in single treatments, and interactions resulted in two synergistic and eight additive responses. Metarhizium-based treatments reduced WFT survival by 93–99.6 % when late mortality by mycosis was considered. Halving the number of released predators did not significantly reduce efficacy (86–96 vs. 76–88 % thrips reduction), and when Orius was introduced to target L1 of WFT, 96–98 % reduction was achieved while only 71–89 % for L2. Early release of O. laevigatus and combination with soil application of NeemAzal-T and/or entomopathogens can be a successful and reliable biocontrol strategy for WFT.

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References

  • Angeli G, Baldessari M, Maines R, Duso C (2005) Side-effects of pesticides on the predatory bug Orius laeviagtus (Heteroptera: Anthocoridae) in the laboratory. Biocontrol Sci Technol 15:745–754

    Article  Google Scholar 

  • Ansari M, Tirry L, Moens M (2004) Interaction between Metarhizium anisopliae CLO 53 and entomopathogenic nematodes for the control of Hoplia philanthus. Biol Control 31:172–180

    Article  Google Scholar 

  • Ansari MA, Shah FA, Whittaker M, Prasaad M, Butt TM (2007) Control of western flower thrips (Frankliniella occidentalis) pupae with Metarhizium anisopliae in peat and peat alternative growing media. Biol Control 40:293–297

    Article  Google Scholar 

  • Ansari MA, Brownbridge M, Shah FA, Butt TM (2008) Efficacy of entomopathogenic fungi against soil-dwelling life stages of western flower thrips, Frankliniella occidentalis, in plant-growing media. Entomol Exp Appl 127:80–87

    Article  Google Scholar 

  • Berndt O, Meyhöfer R, Poehling H-M (2004) The edaphic phase in the ontogenesis of Frankliniella occidentalis and comparison of Hypoaspis miles and Hypoaspis aculeifer as predators of soil-dwelling thrips stages. Biol Control 30:17–24

    Article  Google Scholar 

  • Bielza P, Quinto V, Fernandez E, Gravalos C, Contreras J (2007) Genetics of spinosad resistance in Frankliniella occidentalis (Thysanoptera: Thripidae). J Econ Entomol 100:916–920

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012) 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 87:803–812

    Article  CAS  PubMed  Google Scholar 

  • Blaeser P, Sengonca C, Zegula T (2004) The potential use of different predatory bug species in the biological control of Frankliniella occidentalis Pergande (Thysanoptera: Thripidae). J Pest Sci 77:211–219

    Article  Google Scholar 

  • Bonsignore CP, Vacante V (2012) Influences of botanical pesticides and biological agents on Orius laevigatus - Frankliniella occidentalis dynamics under greenhouse conditions. J Plant Prot Res 52:15–23

    Article  Google Scholar 

  • Bosco L, Giacometto E, Tavella L (2008) Colonization and predation of thrips (Thysanoptera: Thripidae) by Orius spp. (Heteroptera: Anthocoridae) in sweet pepper greenhouses in Northwest Italy. Biol Control 44:331–340

    Article  Google Scholar 

  • Brownbridge M (2006) Entomopathogenic fungi: status and considerations for their development and use in integrated pest management. Recent Res Devel Entomol 5:27–58

    Google Scholar 

  • Buitenhuis R, Shipp JL (2005) Efficacy of entomopathogenic nematode Steinernema feltiae (Rhabditida: Steinernematidae) as influenced by Frankliniella occidentalis (Thysanoptera: Thripidae) developmental stage and host plant stage. J Econ Entomol 98:1480–1485

    Article  CAS  PubMed  Google Scholar 

  • Cloyd RA (2009) Western flower thrips Frankliniella occidentalis management on ornamental crops grown in greenhouses: have we reached an impasse? Pest Technol 3:1–9

    Google Scholar 

  • Down RE, Cuthbertson AGS, Mathers JJ, Walters KFA (2009) Dissemination of the entomopathogenic fungi, Lecanicillium longisporum and L. muscarium, by the predatory bug, Orius laevigatus, to provide concurrent control of Myzus persicae, Frankliniella occidentalis and Bemisia tabaci. Biol Control 50:172–178

    Article  Google Scholar 

  • Ebssa L, Borgemeister C, Poehling HM (2006) Simultaneous application of entomopathogenic nematodes and predatory mites to control western flower thrips Frankliniella occidentalis. Biol Control 39:66–74

    Article  Google Scholar 

  • Faraway JJ (2006) Extending the Linear Model with R: Generalized Linear. Mixed Effects and Nonparametric Regression Models. Chapman & Hall/CRC, Boca Raton, USA

    Google Scholar 

  • Gao Y, Reitz SR, Wang J, Tamez-Guerra P, Wang E, Xu X, Lei Z (2012) Potential use of the fungus Beauveria bassiana against the western flower thrips Frankliniella occidentalis without reducing the effectiveness of its natural predator Orius sauteri (Hemiptera:Anthocoridae). Biocontrol Sci Techn 22:803–812

    Article  Google Scholar 

  • Goettel MS, Inglis GD (1997) Fungi: Hyphomycetes. In: Lacey L (ed) Manual of Techniques in Insect Pathology. Academic Press, San Diego, pp 213–249

    Chapter  Google Scholar 

  • Herron GA, James TM (2005) Monitoring insecticide resistance in Australian Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) detects fipronil and spinosad resistance. Aus J Entomol 44:299–303

    Article  Google Scholar 

  • Holmes ND, Bennison JA, Maulden KA, Kirk WDJ (2012) The pupation behaviour of the western flower thrips, Frankliniella occidentalis (Pergande). Acta Phytopathol Entomol Hungarica 47:87–96

    Article  Google Scholar 

  • Islam MT, Omar DB (2012) Combined effect of Beauveria bassiana with neem on virulence of insect in case of two application approaches. J Anim plant Sci 22:77–82

    Google Scholar 

  • Islam MT, Castle SJ, Ren S (2010) Compatibility of the insect pathogenic fungus Beauveria bassiana with neem against sweetpotato whitefly, Bemisia tabaci, on eggplant. Entomol Exp Appl 134:28–34

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Karanja J, Poehling H-M, Pallmann P (2015) Efficacy and dose response of soil-applied Neem formulations in substrates with different amounts of organic matter, in the control of whiteflies, Aleurodes proletella and Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). J Econ Entomol 108:1182–1190

    Article  PubMed  Google Scholar 

  • Lacey L, Frutos R, Kaya H, Vail P (2001) Insect pathogens as biological control agents: Do they have a future? Biol Control 21:230–248

    Article  Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized Linear Models, 2nd edn. Chapman & Hall/CRC, Boca Raton, USA

    Book  Google Scholar 

  • Medina P, Smagghe G, Budia F, Tirry L, Vin E (2003) Toxicity and absorption of azadirachtin, diflubenzuron, pyriproxyfen, and tebufenozide after topical application in predatory larvae of Chrysoperla carnea (Neuroptera: Chrysopidae). Environ Entomol 32:196–203

    Article  CAS  Google Scholar 

  • Mitchell PL, Gupta R, Singh AK, Kumar P (2004) Behavioral and developmental effects of neem extracts on Clavigralla scutellaris (Hemiptera:Heteroptera:Coreidae) and its egg parasitoid, Gryon fulviventre (Hymenoptera: Scelionidae). J Econ Entomol 97:916–923

    Article  CAS  PubMed  Google Scholar 

  • Mohan MC, Reddy NP, Devi UK, Kongara R, Sharma HC (2007) Growth and insect assays of Beauveria bassiana with neem to test their compatibility and synergism. Biocontrol Sci Techn 17:1059–1069

    Article  Google Scholar 

  • Niassy S, Maniania NK, Subramanian S, Gitonga LM, Mburu DM, Masiga D, Ekesi S (2012) Selection of promising fungal biological control agent of the western flower thrips Frankliniella occidentalis (Pergande). Lett Appl Microbiol 54:487–493

    Article  CAS  PubMed  Google Scholar 

  • Nyasani JO, Subramanian S, Poehling H-M, Maniania NK, Ekesi S, Meyhöfer R (2015) Optimizing western flower thrips management on French beans by combined use of beneficials and imidacloprid. Insects 6:279–296

    Article  PubMed  PubMed Central  Google Scholar 

  • Otieno JA, Pallmann P, Poehling H-M (2016) The combined effect of soil-applied azadirachtin with entomopathogens for integrated management of western flower thrips. J Appl Entomol 140:174–186

    Article  CAS  Google Scholar 

  • Pozzebon A, Boaria A, Duso C (2015) Single and combined releases of biological control agents against canopy- and soil-dwelling stages of Frankliniella occidentalis in cyclamen. BioControl 60:341–350

    Article  CAS  Google Scholar 

  • Premachandra WTSD, Borgemeister C, Berndt O, Ehlers RU, Poehling H-M (2003a) Combined releases of entomopathogenic nematodes and the predatory mite Hypoaspis aculeifer to control soil-dwelling stages of western flower thrips Frankliniella occidentalis. BioControl 48:529–541

    Article  Google Scholar 

  • Premachandra WTSD, Borgemeister C, Berndt O, Ehlers UE, Poehling H-M (2003b) Laboratory bioassays of virulence of entomopathogenic nematodes against soil-inhabiting stages of Frankliniella occidentalis Pergande (Thysanoptera: Thripidae). Nematology 5:539–547

    Article  Google Scholar 

  • R Core Team (2016) R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Rahman T, Spafford H, Broughton S (2011) Single versus multiple releases of predatory mites combined with spinosad for the management of western flower thrips in strawberry. Crop Prot 30:468–475

    Article  Google Scholar 

  • Reitz SR, Gao YL, Lei ZR (2011) Thrips: Pests of concern to China and the United States. Agric Sci China 10:867–892

    Article  Google Scholar 

  • Sanchez JA, Alcazar A, Lacasa A, Llamas A, Bielza P (2000) Integrated pest management strategies in sweet pepper plastic houses in the Southeast of Spain. IOBC/WPRS Bull 23:21–30

    Google Scholar 

  • Shapiro-Ilan DI, Cottrell TE, Mizell RF, Horton DL, Behle RW, Dunlap CA (2010) Efficacy of Steinernema carpocapsae for control of the lesser peach tree borer, Synanthedon pictipes: Improved aboveground suppression with a novel gel application. Biol Control 54:23–28

    Article  Google Scholar 

  • Shipp JL, Wang K (2003) Evaluation of Amblyseius cucumeris (Acari: Phytoseiidae) and Orius insidiosus (Hemiptera: Anthocoridae) for control of Frankliniella occidentalis (Thysanoptera: Thripidae) on greenhouse tomatoes. Biol Control 28:271–281

    Article  Google Scholar 

  • Silveira LCP, Bueno VHP, van Lenteren JC (2004) Orius insidiosus as biological control agent of thrips in greenhouse chrysanthemums in the tropics. Bull Insectol 57:103–109

    Google Scholar 

  • Skinner M, Gouli S, Frank CE, Parker BL, Kim JS (2012) Management of Frankliniella occidentalis (Thysanoptera: Thripidae) with granular formulations of entomopathogenic fungi. Biol Control 63:246–252

    Article  Google Scholar 

  • Steiner MY, Spohr LJ, Goodwin S (2011) Relative humidity controls pupation success and drop** behaviour of western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Aust J Entomol 50:179–186

    Article  Google Scholar 

  • Tedeschi R, Alma A, Tavella L (2001) Side-effects of three neem (Azadirachta indica A. Juss) products on the predator Macrolophus caliginosus Wagner (Heteroptera: Miridae). J Appl Entomol 125:397–402

    Article  CAS  Google Scholar 

  • Thoeming G, Draeger G, Poehling H-M (2006) Soil application of azadirachtin and 3-tigloyl-azadirachtol to control western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae): translocation and persistence in bean plants. Pest Manag Sci 62:759–767

    Article  CAS  PubMed  Google Scholar 

  • Weintraub PG, Pivonia S, Steinberg S (2011) How many Orius laevigatus are needed for effective western flower thrips, Frankliniella occidentalis, management in sweet pepper? Crop Prot 30:1443–1448

    Article  Google Scholar 

  • Williams CD, Dillon AB, Harvey CD, Hennessy R, Namara LM, Griffin CT (2013) Control of a major pest of forestry, Hylobius abietis, with entomopathogenic nematodes and fungi using eradicant and prophylactic strategies. Forest Ecol Manag 305:212–222

    Article  Google Scholar 

  • Xu X, Borgemeister C, Poehling H-M (2006) Interactions in the biological control of western flower thrips Frankliniella occidentalis (Pergande) and two-spotted spider mite Tetranychus urticae Koch by the predatory bug Orius insidiosus (Say) on beans. Biol Control 36:57–64

    Article  CAS  Google Scholar 

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Acknowledgments

The authors would like to express their gratitude to Trifolio-M GmbH (Lahnau, Germany) for providing NeemAzal-T, e-nema GmbH (Raisdorf, Germany) for providing Steinernema carpocapsae (Nemastar®), and the International Centre of Insect Physiology and Ecology (icipe) (Nairobi, Kenya) for supplying Metarhizium anisopliae isolate ICIPE-69. The study was supported by a grant from the German Academic Exchange Service (Deutscher Akademischer Austauschdienst-DAAD).

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  1. Institute of Horticultural Production Systems-Department of Phytomedicine, Leibniz Universität Hannover, Herrenhäuser Strasse 2, 30419, Hannover, Germany

    Jacinter Atieno Otieno & Hans-Michael Poehling

  2. Department of Mathematics and Statistics, Lancaster University, Lancaster, LA1 4YF, UK

    Philip Pallmann

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  1. Jacinter Atieno Otieno
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Correspondence to Jacinter Atieno Otieno.

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Otieno, J.A., Pallmann, P. & Poehling, HM. Additive and synergistic interactions amongst Orius laevigatus (Heteroptera: Anthocoridae), entomopathogens and azadirachtin for controlling western flower thrips (Thysanoptera: Thripidae). BioControl 62, 85–95 (2017). https://doi.org/10.1007/s10526-016-9767-7

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