813 2017 Monitoring is based 7 7 , 4 , 1 Compared with yellow sticky traps, 10 Monitoring information on the development of WFT However, in high-value ornamental crops or in crops 6 9 , 8 Correspondence to: S Mouden, Research Group Plantistry, Ecology Institute and of Phytochem- Biology, Leiden University, POlands. E-mail: Box [email protected] 9505, 2300 RA, The Nether- Research Group Plant Ecology and Phytochemistry, InstituteUniversity, The of Netherlands Biology, Leiden ∗ years after Morse and Hoddle, we aimedge to review the about current knowl- WFT controlcontrol in and relation host toResulting IPM, plant knowledge stressing resistance biological gaps asapproaches, are with areas emphasis identified, on of and theare major emerging new discussed. ‘omics’ progress. techniques, innovative WFTdevelopment biology of knowledge-based and IPM approaches,been ecology, have extensively already reviewed fundamental elsewhere. to the with a high threat ofWFT virus prevails. transmission, a near-zero tolerance for 22.1 WFT CONTROL TACTICS Monitoring In order effectively to manageoutbreaks, current early and intervention anticipate and future pest thethresholds are development critical. of However, economic theimpact assessment of of the WFT economic only has only a recently few begunestablished, economic such to as damage develop. in Therefore, thresholds tomato,strawberry. pepper, for eggplant, cucumber WFT and have been on regular visual scouting ofon WFT the adults use on of flowers and sticky fruits traps. or population levels relative to the economic thresholds is assessed to decide on the employment of control tactics. 3 , 2 (Pergande), published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. Therefore, in the 7 – 5 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. ; integrated pest management; biological control; resistance; ‘omics’ techniques Direct damage results from 1 Kryss Facun Sarmiento, Peter GL Klinkhamer and Frankliniella occidentalis * Pest Management Science Pest Management Science Frankliniella occidentalis thrips; Control of WFT mainly relied on frequent use of insec- 4

this led to a worldwide destabilisation of IPM programmes 1

Kirsten A Leiss © 2017 The Authors. This is an open access articlemedium, under provided the the terms original of work the is Creative properly Commons cited. Attribution License, which permits use, distribution and reproduction in any Their small size,tive affinity potential and forpressure. high enclosed dispersal spaces, capability high cause reproduc- a high pest Western flower thrips (WFT), forms a keymopolitan agri- and and polyphagous invader horticulturaland is greenhouse pest abundant crops. worldwide. ineconomically many WFT This important field developed cos- pests into owingtial to one and its of concurrent vastthe lack the damage pesticide-dominated poten- of most methods. viable management alternatives to 1 INTRODUCTION Western flower thrips (WFT)legislation has is caused one a dramatic ofThe shift the development in of most pest alternative management economicallytactics strategies, strategies in important pushing integrated is for pest pest therefore tactics management insectsmajor an that (IPM) progress. of are of issue WFT, Knowledge less of many with gaps reliable the increasing are crops ontechnologies. focus identified chemicals. urgency. worldwide. Successful on and This biological programmes Recent innovative control paper are approaches EU andbeneficial, reviews emphasised, host cost-effective most and plant highlighting the likely environmentally resistance the sound main as generated advances foundations areas control © are when in 2017 of incorporated. ‘omics’ The preventive Authors. and therapeutic strategies with mutually Keywords: Abstract thrips: past, present and future Sanae Mouden, (wileyonlinelibrary.com) DOI 10.1002/ps.4531 Integrated pest management in western flower Review Received: 26 August 2016 Revised: 18 December 2016 Accepted article published: 27 January 2017 Published online in Wiley Online Library: 28 February for many crops. To emphasise thetion development of and alternative implementa- control measures, the EUon issued sustainable new use of legislation pesticides (Directive 2009/128/EC),on as regulation well of as plant protection products (EC No. 1107/2009). Ten ticides. This overuse of pesticidesWFT has resistance led to to major the insecticidemarketable development groups, of residue crops, problems toxicity on towardsisms beneficial and contamination non-target of organ- the environment. feeding and oviposition on plantindirect leaves, damage flowers is and caused fruits, by virus while spotted transmission, wilt of virus which tomato (TSWV) is economically the most important. framework of integrated pestmultiple management complementary (IPM) tactics programmes, itoring, are cultural, necessary, physical including andresistance, mon- biological mechanical control and measures, semiochemicals, along hostjudicious with use plant the of pesticides.have IPM started programmes for to controlcontinued develop of injudicious WFT mainly use of forof pesticides protected WFT resulted and crops. associated in viruses a However, whileand depleting resurgence competitive its species. natural As enemies Morse andago, Hoddle reviewed 10 years 39 The et al. 42 Identi- 34 : 813–822 Transgenic 73 Interestingly, Expression of 38 36 , 40 2017; 35 , chlorogenic- and , bioassays. glycoprotein inter- 33 Nevertheless, these , N 31 23 in vitro Pest Manag Sci Developing an ecometabolomic 33 Jacobaeavulgaris WFT reached maximal reproductive 43 -alanine in carrot. 𝛽 However, the potential interference of these 41 were strongly stimulated upon exposure of plants to thrips. Purified cystatin and equistatin, when incorporated PDF1.2 37 and 2.3.2 Chemical hostPlant plant resistance chemical defenceondary can metabolites. arise Primary fromcals, metabolites, are both generally as beneficial primary for nutritional thrips. and However,tions at chemi- low they sec- concentra- can also beent involved crops, in low WFT concentrations resistance. ofrelated Among aromatic with differ- reduced amino WFT acids feeding were damage. cor- feroluylquinic acid in chrysanthemum, acylsinapic sugars acid, in luteolin tomato and and into artificial diets, reduced WFT oviposition rates. Cysteine PI transgenic potatoequistatin were plants deterrent to thrips, overexpressing while overexpression of stefin kinino- gen A domain 3 or and cystatin C did not inhibit WFT. approach comparing metabolomic profilesceptible of plants, resistant compounds and for constitutive sus- identified WFT and resistance validated were in subsequent chrysanthemums, overexpressing multicystatin,teinase inhibitor, a did not potato show a pro- clear effect on WFT fecundity. multidomain protease inhibitors in potatoresistance significantly to improved thrips. some of these metabolites not onlyon have WFT shown a but negative effect alsoantioxidant functions have in received human health considerable prevention. attention for their 2.3.3 Transgenic plants Plant proteasedefence inhibitors compounds (PIs) reducingfor are the insect growth naturally availability anding of development. occurring an Transgenic amino anti-elastase alfalfa, plant express- acids proteasedamage. inhibitor, noticeably delayed WFT universal compounds do not provide anylikely uniqueness and to are be not effectivemajority in of resistance studies on focusin their plant on defence. own. the Hitherto, Therefore, rolecal few the of host studies plant have secondary resistance investigated metabolites to chemi- themum WFT. varieties, In isobutylamide was a suggested study towith on be WFT different host associated plant chrysan- resistance. feredwithTSWVacquisitionandtransmissionbyWFTlarvae. multidomain proteins withpractical basic application cell for pest functions managementresistance, has so transgenic far. hindered Targeting tomato a virus expressing G use of transgenic plants, alternatedadditional or strategies, simultaneously is used recognised with thrips as and a tospovirus promising management approach byHowever, for the highly scientific restrictive community. politicallimit and the regulatory frameworks commercialisationEurope. of genetically modified crops in 2.3.4 Induced resistance In additiondefences to as constitutive aimise response costs. defences, Induced tocross-communicating plants defences pest signalling are pathways. use attack, The regulatedsalicylic plant inducible presumably by acid hormones to a (SA)(ET), network and min- trigger of jasmonic naturally acidplants occurring (JA), from chemical as insects responsesimportant well protecting and role in as pathogens. defence against ethylene thrips. TheVSP2 The JA-responsive JA genes pathway plays an fied compounds included jacobine, jaconine andcoside in kaempferol the glu- wild plant species Arabidopsis 29 23 25 27 11 www.soci.org S Mouden © 2017 The Authors. However, 30 In contrast, high 20 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. Fertilisation increases Screening greenhouse WFT incidence in pro- 21 14 , 15 13 12 Instead, the latter provided clear indi- 28 Similarly, high levels of aromatic amino 32 , 22 31 High rates of phosphorus favoured thrips Flowering chrysanthemums as trap plants UV-reflective mulch repelled WFT colonis- 24 , Pest Management Science 26 18 17 Irrigation, creating a less favourable environment 19 , 18 A combination of a positive-pressure force ventilation 16 for thrips, reduced numbers of WFT adults. cations that resistance wasplant composition. mainly influenced by chemical host ing adults through interruptionbehaviour. of orientation and host-finding wileyonlinelibrary.com/journal/ps Induction of type VI glandular trichomes inmonate response application to methyljas- trapped higher numbers of WFT. 2.3.1 Morphological defenceThe structures surface of a host plantmorphological can traits such serve as as waxy a cuticles physical and/ortures epidermal barrier struc- through including trichomes.lated WFT with damage the amount was of negatively epicuticular wax corre- on gladiolus leaves. 2.3 Host plantPlants resistance and insects have coexisted forIn more the than course 350 of evolution, million plants years. have evolvedmechanisms, a variety constitutive of and defence inducible, toand this reduce has insect led attack, toresistance involves host a plant large resistance. web of Theby complex study interactions, morphological of mediated and host chemical plant traitsof that damage influence caused the by amount defensive traits pests. plays Understanding a critical the role inenhanced nature designing protection crop of against varieties pests. with plant Intercropping French beans with sunflower,compromised potato bean or yield baby but corn reducedincreasing damage marketable to yield. the bean pods, Trap crops draw WFTtrolled away more from easily. the crop, where it can be con- A positive correlationabundance between was phenylalanine observed in and onebut female study not on WFT in field-grown another. tomatoes, 2.2 Cultural, mechanicalSince and physical control ancient of WFT time,physical farmers practices have for thetices been management such relying of as on pests.form removing Sanitary cultural the prac- weeds, or first old line plant of material WFT and defence. debris Based on WFT samplings, modelstiongrowthandspreadofTSWVhavebeendevelopedaspotential for predictions of WFTdecision popula- tools for IPM programmes. blue traps have shown to catchalso more be WFT; used yellow for sticky monitoring traps aphids, can use whiteflies and of leafminers. The monitoring toolssemiochemicals as has lures that been significantly increase thrips expanded catches. by the addition of acids promoted WFT larval development in different vegetables. plant development and growth butIncreased also levels of affects nitrogen WFT fertilisation increased abundance. WFTnumbers population in ornamentals. system with insect-proofinvasion screens by did thrips. not prevent greenhouse openings prevented WFT immigrationrequires into optimisation protected crops of but ventilation. lowered WFT damage in a vegetative chrysanthemum crop. relative humidity favouredulated WFT pupation larval in development and the stim- plant canopy. development but did not lead to increased thrips damage. other studies did not observe anying correlation damage between and WFT morphological feed- traitsdry weight such and leaf as area. hairiness, leaf age, tected tomato was reducedscreens. by 20% using greenhouse window

814 815 59 64 67 (for- Orius In con- Several against showed )signifi- 57 72 Treatment 63 Metarhizium – 69 , 61 Success of suppressed WFT 59 , , as well as the rove ), are commercially Verticillium , in the presence of 58 B. bassiana Although a key natu- are the only two par- is a better predator on Heterorhabditis 60 , repeated applications 68 , Stratiolaelaps scimitus , 67 and S. feltiae spp. are relatively expensive O. insidious (formerly 56 , A. swirskii 55 Beauveria bassiana Atheta coriaria Orius wileyonlinelibrary.com/journal/ps C. americensis has been shown to induce WFT resis- Gaeolaelapsaculeifer and have been tested to evaluate their use Steinernema (formerly )and Orius has been successful in all-year-round biological Besides the direct effects, nematodes, infecting WFT residing within flower Macrocheles robustulus Lecanicillium lecanii O. laevigatus 71 , 59 70 While foliar application of and 66 , Ceranisus menes 65 Dalotia coriaria Hypoaspismiles O. laevigatus , commonly known as pirate bugs, are known to be gener- Thripinema Entomopathogenic fungal conidia infect thrips by penetrating produced as biocontrol agents against WFT pupae. beetle merly predation, thrips control isence not of whitefly, negatively while in affected contrast whitefly by in the the presence pres- of thrips. sublethal effects on the progeny of treated WFT adults. a wetting agent, has notadults been shown and to larvae successfully in control WFT chrysanthemum their cuticle toIn obtain general, nutrients adult forpupal thrips growth stages, and are possibly reproduction. fungal more because inoculum. susceptible In moulting addition, thanmay avoids larvae larval have delay contact thicker and penetration cuticles, with ent of which fungal fungus. strains Foliar belonging to applications of differ- cantly reduced thrips populationsfloral in greenhouse crops. vegetable and soil-inhabiting WFT pupae produced low andresults. inconsistent control 2.4.4 Parasitoids To date, Under laboratory conditions, thesefirst-instar parasitic larvae, wasps resulting oviposit in into deathever, slow of wasp the development time prepupal hinders stage. efficient WFT How- control. 2.4.5 Entomopathogens Entomopathogens used as WFT biocontrol agents consist of nema- todes and fungi. The use ofin various the nematode nematode species genera and strains 2.4.2 Predatory bugs Orius alist predators, preying oninsect adults species and such larvae as of aphids,Several whiteflies, a species spider wide of mites range and of thrips. Oviposition of tance in tomato through wound response. 2.4.3 Soil-dwelling predators Most research on WFTval biocontrol stages. However, has WFT focused spend one-third onthe of soil. adult their Different life soil-dwelling and as predatory lar- pupae mites havegated, in of been which investi- asitoid wasps investigated for their potential to control WFT. with buds and foliar terminals,female was WFT. This non-lethal treatment and was insufficient caused for sterility control of of WFT. in ornamentals depends on the complexity of flower structure. ral enemy in biocontrol of WFT, to mass rear. successfully reduced thrips damage in cucumber. anisopliae against WFT. Observations from field and glasshousein experiments sweet pepper demonstrated that almost to extinction, butshort-day conditions failed in to autumn as control they WFT enter diapause. properly under trast, control of WFT in vegetables and ornamentals. . 49 43 A. A. N provided Amblyseius) has therefore -methyl (ASM), A. montdorensis S Thrips are not the Compared with in control of WFT in and A. swirskii have been recorded 53 49 , published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. In addition to control (formerly spp.) and pirate bugs Induced resistance has A. swirskii 48 , deficient in JA, in com- 49 47 In contrast to WFT, TSWV in summer, likely owing to Thrips can also consume 44 A. swirskii def-1 52 Amblyseius as a WFT biocontrol agent is also Treatments with exogenous elic- Neoseiulus A. degenerans Amblyseius , 45 and N. cucumeris In chrysanthemum, induced SA-regulated gene expression. has recently been investigated. Supplying A. swirskii : 813–822 © 2017 The Authors. proved to be a better WFT predator than in 50 A. swirskii Next to being an efficient predator of WFT, Pest Management Science , 73 54 also provides control of whiteflies. Although the sp.). 2017; Arabidopsis A. swirskii A. swirskii Treatment of tomato with acibenzolar- , , which primarily feed upon first-instar larvae. Owing to Efficiency of A. limonicus A. swirskii 46 is easily reared, which allows economic mass production. eggs, and female predators were observed preferentially to 51 spp.). Several species of Amblyseius barkeri Artemia Orius proved to be effective predators of WFT. pollen improved the performance of chrysanthemum, as did the addition of decapsulatedcysts brine ( shrimp infection in Pest Manag Sci become the main predator usedvegetables for and biological ornamentals control worldwide. of WFT in Since its commercial introduction in 2005, The resulting antagonisticSA-regulated defence interaction systemsenhanced between in the the response performanceplants JA- to over of TSWV and uninfected WFT ones. infection preferring TSWV-infected Integrated pest management in western flower thripsperformance in the tomato mutant www.soci.org parison with the mutant expressing a 35S::prosysteminconstitutively transgene, activating JA defence. of WFT, presence of whitefly can lead to a short-term escape of thrips from cucumeris sweet pepper, as femalesand showed a kill higher WFT propensity to larvae. attack a functional analogue ofnot influence SA, WFT reduced population densities. TSWV incidence, but did itors activate the naturalenhancing defensive response resistance of a toresulted plant, in thrips. a thereby decreased preference, Applicationof performance WFT. and of abundance JA in tomato cucumeris the inadequate control achieved,been a number studied of in other ordersuch mites as to have find a superior WFT predator. Species ( as predators offor WFT, their and efficacy. The variouswere first species predatory have mites used been for assessed WFT control 2.4.1 Predatory mites The principal arthropod predators associated withcontrol WFT biological are phytoseiid mites ( 2.4 Biological control Biological control uses themies augmentative release as of well natural asdance ene- conservation and approaches efficiency. toknown sustain A to their large attack abun- WFT, numbermacrobials, which which of can include be natural predators separated andbials, enemies into parasitoids, which two are and are groups: micro- subdividednematodes. into Table 1 enthomopathogenic summarises fungi the mostavailable and biocontrol common agents commercially used against WFT. recently gained more interest andconjunction might with be other of IPM particular approaches. value in oviposit at sites without thrips, or tosites, kill presumably more thrips to at protect oviposition their offspring. swirskii influenced by host plantdensities hinder species, mite and performance. here increased trichome best food source for mites. Therefore,tal the addition food of to supplemen- swirskii higher thrips control than a better survival, while bothwinter. predators showed similar efficacy in B. et al. and or the S. feltiae : 813–822 H. aculeifer 73 available Commercially In contrast, the with the respec- 2017; D. coriaria 81 , M. brunneum Likewise, laboratory 59 G. aculeifer achieved good WFT control in O. laevigatus Pest Manag Sci increased mortality of WFT pupae Combinations of different predatory S. feltiae 82 nematodes with the foliar-dwelling mite S. feltiae did not reduce thrips numbers in ornamentals It is apparent that combinations of biocon- Pupae 2002 Canada PupaePupaePupae 2008 1995 Europe 1994 Europe Europe LarvaeLarvae 1993 1985 Worldwide Europe LarvaeLarvaeLarvae 2007 2010–2011 2010–2011 The Netherlands The The Netherlands Netherlands Larvae 2012 The Netherlands 84 Concurrent use of the soil-dwelling mite provided superior control in green bean compared Parasitises larvaeParasitises larvae 1996 1996 The Netherlands The Netherlands First-instar larvaeFirst-instar larvae 1995 1981 Worldwide Worldwide feltiae Larvae and adults 1900s North America Larvae and adultsLarvae and adultsLarvae and adultsLarvae and adults 1900s 1991 Worldwide 1993 2008–2009 Europe Australia EU and USA 83 Adults most susceptibleAdults most susceptibleAdults most susceptible 2012 2012 Europe 2012 The Netherlands EU and USA achieved higher control of WFT compared with single Pupae, prepupae and larvae 2005 Worldwide First- and second-instar larvae 2005 Europe Heterorhabditis cycle. Hence, combinations of foliaragents targeting and all soil-dwelling WFT life biocontrol stages havetaneous been investigated. Simul- treatment ofpredators different with mites the or soil pirate predators bugs as foliage with the nematode in green bean. nematode S. beyond that caused by foliage predators alone. mites with the nematode cyclamen, while combinations of tive nematodes failed to control thrips. trol agents for controlmanagement of and WFT fine-tuning suiting are the crop promising in but question. require careful 2.5 Behavioural control An important focus in applied pestadult insect control behaviour is using semiochemicals the functioning manipulation as of signal compounds. Pheromones serve forbetween intraspecific arthropods, communication while allelochemicals mediateinteractions. plant–insect Semiochemicals are used aswell as lures for for control purposes. monitoring as combinations of different soil-dwelling predators with did not improvepredators with thrips the entomopathogenic control, fungi bassiana while combinations oftreatments. these use of N. cucumeris with individual releases. www.soci.org S Mouden © 2017 The Authors. together O. laeviga- Amblyseius barkeri Amblyseius degenerans Amblyseius californicus Amblyseius swirskii Ceranisus americensis Amblyseius cucumeris Amblyseius andersoni Ceranisus menes Steinernema feltiae Amblyseius montdorensis Amblydromalus limonicus Orius insidious Lecanicillium lecanii Metarhizium anisopliae Beauveria bassiana Isaria fumosorosea Orius laevigatus Atheta coriaria Orius albidipennis Orius majusculus Orius armatus Macrocheles robustulus Hypoaspis aculeifer Hypoaspis miles 76 , 75 . Information retrieved from the Biopesticide Database of the University of Hertfordshire (www Simultaneous use A. swirskii 77 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. Fungi Rove beetle Minute bugs F. occidentalis Classification Type of agent WFT stage affected First use , a generalist predator to control Major constraints to the use of 80 , 73 70 In contrast, a combination of 78 , Soil dwellers Mites 58 Pest Management Science in laboratory trials led to negative interactions Combinations of the entomopathogenic fun- with predatory mites did not inhibit or enhance Recently, the use of endophytic fungi, developing 79 74 Biological control agents of Macrolophus pygmaeus N. cucumeris B. bassiana and Thrips generally complete their life cycle within 2 weeks, causing .herts.ac.uk) Predators Crop dwellers Mites (foliar) ParasitoidsEntomopathogens Nematodes Parasitic wasp Table 1. gus the control of WFT, becausehindered by fungal mite dissemination grooming. seemed to be within plant tissues without causing diseaseexplored symptoms, has for been WFTpreference control. or development So have been observed. far, no negative effects on WFT several generations to overlap during a single crop production tus aphids, achieved enhanced controlsweet of both pepper. thrips and aphids in with on WFT control through intraguild predation. wileyonlinelibrary.com/journal/ps 2.4.6 Combinatorial useCombinatorial of biological control treatmentsarthropods of or natural arthropodsalternative with enemies or entomopathogens with back-up areand treatments. compatibility different used of This treatments. Application as of requires careful timing formulations of entomopathogenic fungifoliar applications, are but now their efficacy availableowing has for to been inconsistent, varying likely lations ambient targeting humidity the andin soil temperature. potted stage Formu- chrysanthemum. have shown promising results entomopathogenic fungiagents as remain augmentative the difficultiesformulation. biological in control mass production, storage and of predatory mites and pirateWFT bugs in greenhouse did crops, have but the a effect negativeone was effect no predator greater on than alone. using

816 817 The 100 96 , 95 101 Spinosad, a natural by attracting thrips cutflowers cutflowers cutflowers chrysanthemum, rose, cutflowers, lettuce, cucumber, strawberry chrysanthemum, rose, cutflowers, lettuce, strawberry cutflowers, lettuce, cucumber, strawberry strawberry cutflowers 102 , 7 New, narrow-spectrum Chrysanthemum, rose, Capsicum, Capsicum, rose, – 4 4 , 1 Combination of dodecyl acetate M. anisopliae 98 , wileyonlinelibrary.com/journal/ps 97 The use of broad-spectrum insecticides, Use of LUREM-T together with the WFT 7 , 4 increased the abundance of the latter. 99 receptor chloride channel receptor O.laevigatus Currently, the three commercially available WFT semiochemicals Management of thrips has relied on the application of insec- monoterpenoid phenols thymol andfeeding carvacrol as well exhibited as a both oviposition a deterrent effect to WFT. including pyrethroids,carbamates, neonicitinoids, kills native organophosphates outcompeting thripsenemies and species disrupting WFT and management. natural are mainly used as lures in conjunction withthrips sticky card constantly traps. Adult explore their hostduction range by for utilising feeding different andsemiochemicals cues, repro- including hold volatiles. great Therefore, promisewell as for ‘lure and thrips kill’ strategies. mass trapping as predator 2.6 Chemical control Chemical control ismethods to among suppress WFT, one particularly foralmost of ornamentals, zero where the damage an tolerance mostof encourages frequently insecticides. intensive Commonly application used usedthrips, insecticides approved for at European management level, are of listed in Table 2. ticides, as has beenrefer described for in further detail. previous reviews, to which we with maldison, an organophosphorous insecticide,val increased mortality lar- of WFT. insecticides for WFTHowever, frequent control applications include ofinsecticides, broad- pyridalyl including and and narrow-spectrum spinosad, have lufenuron. led to the development ‘lure and infect’ strategy employs LUREM-Tof for the entomopathogenic autodissemination fungus to particular traps provided with fungal inoculum. reduced-risk insecticide derived from an actinomycete bacterium, is compatible with naturalmost effective enemies chemical and control currently of provides WFT. the Vertimec Glutamate-gated 92 89 The More 94 , 87 , 93 86 )-lavandulyl R The latter is a sex- (avermectin, milbemycin) published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. 85 Type of compound Trade name Target Crops MethiocarbEsfenvaleraatDeltamethrin Mesurol SumicidinSpirotetramat Decis EC Acetylcholinesterase Sodium channel Movento Chrysanthemum, Sodium rose, channel Chrysanthemum, rose, Acetyl CoA carboxylase Capsicum, Chrysanthemum Thiametoxam Actara Nicotinic acetylcholine Abamectin AzadirachtinPyridalylLufenuron NeemAzalSpinosad Ecdysone Nocturn receptor Match Conserve Protein synthesis Rose, chrysanthemum, Chitin biosynthesis Nicotinic acetylcholine Rose Rose, cutflowers 88 in a dose-dependent way. The latter may represent a plant defence F. occidentalis chemicals spectrum 89 : 813–822 © 2017 The Authors. )-2-methylbutanoate. Broad chemical S Pest Management Science 73 )-verbenone, was described from pine pollen. S Recently, a new potential active ingredient for thrips 2017; 91 Overview of synthetic and natural compounds used against thrips, based on commercial spray advice cards 2015 Synthetic origin Selective Natural origin Pyrethrins Spruzit/Raptol Sodium channel Lettuce, cutflowers, Table 2. lures, volatile ( Pest Manag Sci Volatiles with repellent activities canhost be finding. utilised Applications for disruption ofdeterred of methyl-jasmonate WFT larvae and from cis-jasmone feeding and settling,exposure although repeated resulted in a dose-dependent habituation. While WFT were attracted by pureted linalool as by well as engineered linalool emit- chrysanthemumby linalool plants, glycosides. they were deterred acetate and neryl ( 2.5.2 Allelochemicals Volatiles used to locate plant hosts for feedingbe and applied oviposition can as lures. Various volatilemonoterpenes, phenylpropanoids, scents, pyridines including and a benzenoids, sesquiterpene, attracted adult female 2.5.1 Pheromones Two key pheromones in male WFT were identified: ( Integrated pest management in western flower thrips www.soci.org recently, 7-methyltricosane, a WFT-male-specific cuticularcarbon, hydro- was suggested to inhibit mating. strategy against WFTtive as fragrance a with pooringredient floral taste. of antagonist, Methyl Lurem-TR balancing isonicotinate,Rodenrijs, (Koppert attrac- The the Biological Netherlands), active Systems, isfemale Berkel an WFT en as attractant well for ashost both plants. other male thrips and species and is used to locate ual aggregation pheromoneWFT. attracting The both synthetic analogues maleClacton, Thripline and UK) AMS female and (Syngentause Bioline, ThriPher commercially. (Biobest, Decylrespectively, Westerlo, and are Belgium) dodecyl produced are asdroplets. acetate, in alarm Synthetic 10- pheromones equivalents and inment caused 12-AC and anal WFT take-off larval to rates,rates, increase reduce suggesting their oviposition move- function and as an reduce alarm landing pheromone. The et al. Pseu- , likely 111 : 813–822 Sequenc- 73 110 Addressing the 2017; 34 Thrips tabaci Investigations into endo- ) has been described in 116 In addition, plant secondary Pest Manag Sci 115 Liriomyza trifolii 117 Manipulation of environmental factors may Targeting the vacuolar ATP synthase subunit-B producing the JA analogue coronatine and thus 106 113 For transmission of TSWV, a suite of WFT candidate 114 Rhizobacteria are known to play an important role in 76 , 75 Next to plants, microbials offer a huge source of metabolites into adult thrips. proteins reacting to viral infection has been identified,approach but no RNAi for disruption has yet been developed. 3.4 High-throughput screening Employing genomichowever, as requires a wellfor high-throughput thrips as screening resistance. (HTS) metabolomics Screening system large techniques, numbers of plants for domonas syringae triggering herbivore defence hasplant a defence to potential WFT. to be explored for plant growth, nutrition and health inresponse general. to Genetic the variation in capacity ofbacteria plants opens in the reacting to wayterial these for benefits. beneficial breeding The effect of ofabove-ground plants defence soil directed maximising against microbial insects, bac- such communities as onneeds thrips, still plant to be explored. Similarly, the effect of the bacterium metabolites involved in WFT resistance couldnew be protection used agents to that develop defence enhance mechanisms or activate or the thatwith plants’ may own improved provide selectivity, new minimising modeorganisms. of the actions effects on non-target to be used fornities insect resistance. may Assembly influence ofchemistry the microbial or commu- performance volatile of emission.by thrips fungal Colonisation endophytes through of induced onionowing plant resistance to a seedlings to repellent effect of volatiles. gene resulted in increased WFT mortality and reducedsurviving fecundity of females. Alternatively, symbiont-mediated RNAi,regulating down- an essential tubulin gene, resultedWFT in larvae. high mortality of metabolome, however, allows investigationintegrated of network the underlying complex defence and with mechanisms. genetic Combined approaches, metabolomicserful analyses opportunities provide to pow- identifyto metabolic thrips markers and forIdentification resistance open of up compoundsherbivores, conferring possibilities i.e. cross-resistance, resistance of could to formsistance ‘metabolite a breeding different basis breeding’. programme. for An aand overlap multire- celery of resistance leafminer to ( WFT increase concentrations of resistance-relatedplants, metabolites thereby within enhancingacid, WFT two control. phenolic Rutin compoundsenhanced involved and in upon chlorogenic thrips UV-B resistance, exposure. are phytes increasing resistanceso to far. WFT have not been successful ing thenon-infected salivary WFT led to the gland putative annotation ofin genes transcriptome involved detoxification and inhibition of of plant defence responses. TSWV-infected and availability of WFTwill genome facilitate and the transcriptome developmenteffectors suppressing of sequence or approaches inducing data plant identifying defence responses. thrips 3.3 Metabolomics Metabolomics has aof great compounds potential inmetabolomics to an unbiased has detectapproaches or a mainly using untargeted wide genotypes fashion. beentance, range with So classified restricted far, contrasting as levels to resistant of or comparative resis- susceptible. chrysanthemum. L. ( 106 , 36 , 35 , www.soci.org S Mouden © 2017 The Authors. Sw-5 32 109 , Management 108 ). 103 , 6 , The availability of 5 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. 111 , 110 C. chinense ( However, development of 6 This approach, however, might , Tsw 5 Rotation programmes including 107 5 )and 105 , Various insecticides have been shown 104 104 An RNA interference tool has been devel- Pest Management Science L. chilense ( 112 Sw-7 ), Moreover, the presence of considerable variation in 35 , 32 peruvianum wileyonlinelibrary.com/journal/ps 3.2 Insect genomics Despite their economic importance as‘i5k’ worldwide (5000 crop pests, insect the genome)genomic project and has proteomic tools onlyassembled for recently WFT, and developed including annotated a collection sequences. of Identifying sets of genes or metabolites asintroduction biomarkers of enables novel the insect resistance traits intoa breeding highly lines. resistant In pepper accession, a quantitative traitmapped locus to (QTL), chromosome 6, confers resistancethe to larval WFT development by of affecting thrips. 3.1 Plant genomics While domestication of wildyield plants and through palatability, it selection greatlydiversity, improved leading reduced to phenotypic loss of and insect genetic resistance.fore Wild provide ancestors there- a promisingtraits. source for breeding of WFT resistance In pest management programmes, innovative approaches advanc- ing the prevention and management of pest insectsbeing are sought. constantly The development of non-targetedods, analytical from meth- genomes tothe metabolites, adaptation has been of aapproaches systems-based enable a major comprehensive view approaches. driver of defence mechanisms. Such for The integrative emergence of ‘omic’-based techniques, as wellcomputational as systems, advances provides in a powerful tooltion to in drive crop innova- protection. Understandinggenetic plant–insect variations interactions, among insectvarieties generates populations valuable information and that provides resistant new oppor- tunities crop and technologies by improving our knowledge of complex resistance traits. 3 FUTURE‘OMICS’ DIRECTIONS TECHNOLOGIES OF WFT CONTROL: of WFT resistance to activeas ingredients of has most been chemical classes, extensively revised elsewhere. the thrips genome willelucidate open thrips up new gene powerfulstrategies function based opportunities on and the to molecular develop interaction ofas alternative thrips with well control plants as viruses. rotation schemes does not necessarilyinsecticide focus use. on reducing Therefore, overall economic insecticides damage thresholds should are reached, onlyshould and here be be applications used accuratemies. and if Rotation precise schemes while needcompatible conserving control to approaches. natural be ene- complemented with other be less suitable for polyploidbreeding ornamentals. of At resistant present, cultivars successful known is to limited confer resistance to against TSWV TSWV control. isolates include Genes resistance to WFTvegetables between and accessions, ornamentals, as can observed be in exploited various as well. of WFT insecticide resistancecomprises as resistance reviewed monitoring coupled indifferent with other rotations publications classes among of insecticides. oped using microinjection for delivery of double-stranded RNA to be compatiblecompeting with thrips species. WFT predatory mites, bugs and other entomopathogenic organisms successfully controlled WFTgreenhouse under conditions.

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JP, Binomial sampling of western flowergreenhouse thrips crops infesting using flowering incidence-mean models. 40 Butt TM, A newFrankliniella attractant occidentalis for monitoring western flower thrips (2008). and oviposition of 1 Morse JG and Hoddle MS 2 De Jager CM, Butôt RPT, Klinkhamer PGL, De Jong TJ, Wolff K and van 3 Maris PC, Joosten NN, Peters D and Goldbach RW, Thrips resistance 4 Cloyd RA, Western flower thrips ( 5 Bielza P, Insecticide resistance management strategies against the 6 Gao Y, Lei Z and Reitz SR, Western flower thrips resistance to insec- 7 Demirozer O, Tyler-Julian K, Funderburk J, Leppla N and Reitz SR, 8 Coll M, Shakya S, Shouster I, Nenner Y and Steinberg S, Decision mak- 9 Wang K and Shipp JL, Simulation model for population dynamics of 15 Ben-Yakir D, Teitel M, Tanny J, Chen M and Barak M, Optimizing ven- 16 Escamirosa Tinoco C, Martinez Guitiérrez GA, Aquino Bolanos T 12 Ogada PA, Moualeu DP and Poehling H-M, Predictive models for 13 Northfield TD, Paini DR, Funderburk JE and Reitz SR, Annual cycles 10 Ugine TA, Sanderson JP, Wraight SP, Shipp L, Wang K and11 Nyrop Abdullah ZS, Greenfield BP, Ficken KJ, Taylor JW, Wood M and 14 Nyasani JO, Meyhöfer R, Subramanian S and Poehling H-M, Feeding as in life, one size does not fittrol, all. In strategies order should to be achieve successful tailored con- toent fit production the systems. Controlling requirements pests of is differ- nothas a never trivial been. issue, and The basicconsistent question long-term remains control. of Most how importantly, there one remainsneed achieves the for transdisciplinary approachestices integrating for different control prac- of thrips. ACKNOWLEDGEMENTS The use of trade names in thisof publication providing is solely specific for information. the purpose Thisfunded by review Technology is Foundation STW, part project of 13553. a project REFERENCES Develop- 7 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. However, the availability of the thrips 120 However, a reproducible high-throughput : 813–822 © 2017 The Authors. Recently, a high-throughput phenotyping Pest Management Science 73 119 118 2017; Significant research progress in control of WFT has been made. Pest Manag Sci As from 2014, farmersprinciples in of integrated the pest EU management.various However, are benefits despite obliged expected the to from IPM,dence implement there that the seems IPM to has bedevelop been little their largely evi- respective adopted. methods Manyto as studies pest single-solution seek problems approaches to rather thanbox’. integrating Moreover, vertical these integration into of control an measuresIPM ‘IPM looking of at tool- different pests in one cropping system is scarce. 4 CONCLUSIONS genome sequence providesidentify an gustatory unprecedented or olfactory opportunity receptorsdevelopment. to to form the basis of HTS Integrated pest management in western flower thripsidentification of resistance sourcesing is programmes. vital for resistance breed- www.soci.org method has been described thatof uses WFT automated behaviour. video tracking method assessing thripssystems damage is testing still forfrom lacking. active plants Similarly, or HTS metabolitesthrips-derived microbials cell against lines, are WFT beyondunsuccessful absent. primary until deriving cell Development now. cultures, of has been stable ing and implementing IPM remainstask. a Integrating complex different control knowledge-based tactics is fundamentaling to successful control achiev- of WFT, yet it presents significantClearly, challenges. research into the integration ofative, methods jointly involves cooper- planned activities thata cannot single be pinned methodological down blueprint.ent into How groups develop can protocols scientists andtion of in tests multiple approaches in that differ- sustainable pest allow management while theretaining combina- the capacity toand determine hence the modify individual and contributions improveand progress, these? strategies should For not only optimal be effectiveness integratedmultidisciplinary at inter- research and levels but alsooutcomes in driven cooperation through with applied commercial partnersplinary by research. transdisci- Host plant resistanceSome to breeders already WFT have varieties becomes with differentings; increasingly resistance rat- however, important. for certainthis crops, approach such as is polyploid notsis ornamentals, as has straightforward. been placed Recently, uponcrops. more Nevertheless, biological short empha- crop control cycles and of low WFT thresholds,mentals for in in orna- particular, make protected biological control challenging. 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