Opinion
A
Conceptual
Framework
for
Integrated
Pest
Management
Johan
A.
Stenberg
1,*
,@The concept of integrated pest management (IPM) has been accepted and
incorporated in public policies and regulations in the European Union and
elsewhere,buta holisticscienceofIPMhasnotyetbeendeveloped.Hence,
currentIPMprogramsmayoftenbeconsiderablylessefficientthanthesumof
separately applied individual crop protection actions. Thus, there is a clear
need toformulategeneral principles forsynergistically combiningtraditional
andnovelIPMactionstoimproveeffortstooptimizeplantprotectionsolutions.
Thispaperaddresses thisneed bypresenting a conceptualframework fora
modernscienceofIPM.Theframeworkmayassistattemptstorealizethefull
potentialofIPMandreducerisksofdeficienciesintheimplementationofnew
policiesandregulations.
WhenIsItIntegratedPestManagement?
Many national and intergovernmental bodies have firmly decided that the future officially endorsed paradigm for crop protection will be ‘integrated pest management (IPM)’. For example,aEuropeanUnion(EU)Directive[1]hasobligedallprofessionalplantgrowerswithin theUniontoapplythegeneralprinciplesofIPMsince2014.MosttextbooksdefineIPMasa holistic‘approach’or‘strategy’tocombatplantpestsusingallavailablemethods,withminimal applicationsofchemicalpesticides[2,3].Theaimisnottoeradicate pests,butto manage them,maintainingtheirpopulationsbeloweconomicallyinjuriouslevels[4,5].Puttingthisvision intopracticewouldreducenotonlyfarmers’,consumers’,andtheenvironment’sexposureto toxiccompounds,butalsoproblemscausedbypesticide-resistantpests.
Introduction ofthe IPM concept spurred intense explorationof various actions thatcould contributetoIPMprograms.Atthetimeofwriting,aWebofSciencesearchusingtheterm
‘IntegratedPestManagement’returnsaround50000hits,suggestingthatIPMandassociated issueshaveengagedanarmyofresearchers.However,despitetheexpressedenthusiasmfor IPM,mostcroppingsystemsstilldependonheavyuseofchemicalpesticides[6],andIPMisstill farfrombeingefficientlyresearchedorapplied,probablybecausenoholisticscienceofIPMhas emergedasyet.
Thefounders ofIPM recognizedthat integrating several methods to combat pests would requireinterdisciplinaryresearchprograms[4,5],butmanyinterdisciplinaryresearchprograms withaclaimedobjectivetostudyIPMactuallyfocusonsingleplantprotectionmethods.For example,entomologists,chemicalecologists,andplantbreedersmayapplyaninterdisciplinary approachtogeneratecultivarswithhighindirectresistancetopestinsects,butthiscanhardly beconsideredIPMresearchasitfocusessolelyononeelementofpestmanagement(plants’ intrinsicheritableresistance).Morethanonepestmanagementactionmustbeconsideredto meetthe‘integrated’criterionofIPM.Thus,IproposethatthescienceofIPMshouldbedefined asthesystematicstudyofthecompatibilityandoptimizationofactionsassociatedwithatleast twopestmanagementelements(Box1andFigure1,KeyFigure).Inthisopinionarticle,Ifirst
Trends
Integratedpestmanagementis
glob-allyendorsedasthefutureparadigm
forcropprotection,butinpracticeit
justmeansthatseveralpest
manage-mentelementsarecombined not
integrated.
Differentpestmanagementelements
interactwitheachother,having
syner-gistic or antagonistic effects when
usedtogether.Theemergingscience
ofIPMsystematicallystudiesthe
com-patibility and optimization of the
involvedelements.
Mostinteractions withinIPMinvolve
effects ofplant resistance on other
pestmanagementelements.By
con-trast,biologicalcontrolisaffectedby
almostallotherelements.
1
DepartmentofPlantProtection Biology,SwedishUniversityof AgriculturalSciences,23053Alnarp, Sweden
@
Twitter:@Stenberg_JA
*Correspondence:
[email protected](J.A.Stenberg).
describetheindividualelementsofecologicallybasedIPM,andthenmapresearchroutesto identifyoptimalcombinationsofactionsforsuccessfulIPM.
TheIndividual IPMElements
IntrinsicHeritablePlantResistance
Wildplants have evolved traitsthathelp them resistpests andpathogens eitherdirectlyor indirectly
[7–9].Directdefenses–suchassecondarymetabolites[10],trichomes[11],andwaxlayers[12]–
directlydefyattackers, makingtheplant lessdetectable,attractive,edible,orsusceptibleto infection.Indirectdefenses,bycontrast,attractandrewardthenaturalenemiesofpests,thereby engagingthemas‘bodyguards’[13,14].Planttraitsinvolvedinindirectdefensesincludeodors (oftenpestinduced)thatattractnaturalenemiestoinfestedplants[8],andnectarthatrewardsand sustainsattractednaturalenemiesofpests[15].
Unfortunately,manyresistancetraitshavebeenlostduringthedomesticationofcrops[16,17]. Thereareseveralreasonsforthis,butmostimportantlyresistancewasnotprioritizedduringthe 20thcenturywhenpestproblemscouldbesolvedwithcheapchemicalpesticides.Bycontrast, directdefensetraitswereoftenselectedagainstastheyinterferedwiththetasteandtextureof thecrop.Indirectdefenseswererarelyconsciouslyselectedagainst,butwereignoreddueto lackofawarenessoftheirimportance.
Whilebothdirectandindirectdefensetraitshavebeenwidelylostfrommoderncultivars,recent researchhasshownthatimportanttraitsremaininwildcroprelatives[18–20].Thus,oneofthe mostimportanttasksforresistancebreederswillbetofindandutilizethenaturalvariationin thesetraits–especiallyindirectdefensetraits–inwildcroprelatives,andtransferthemtofuture cultivarstoimprovecrops’intrinsicresistancetopestsandpathogens.
Themultigenenatureofmostresistancemechanismsconstitutesachallengeforsuccessful breeding.Fortunately,increasingresistanceisnowapriority,andnewtechnologiesfortargeted genomeeditingsuchasclusteredregularlyinterspacedshortpalindromicrepeats(CRISPR)/ Cas[21]will aidthisaim, butamajor challengewill betodevelopcultivarswithenhanced resistancetoseveralpests[22].Themostrealisticstrategymaybetoimproveindirectdefenses byenhancingrecruitmentofgeneralistnaturalenemies,whichcancombatdiversepests[19].
PlantVaccination
Plants frequently respond to pest attacks by inducing direct and indirect defenses that efficientlycounter boththecurrentlyattackingpestandpestspeciesthatmayattacklater. This process can be regarded as ‘plant vaccination’ if the defense-inducing organismis relativelyharmlessandtheinduceddefensemakestheplantresistanttoamoredetrimental pest[23].
Plantscanalsobevaccinatedbyexposuretofactorsthatinducea‘primed’state,inwhichthey respondmorerapidlyandstronglytosubsequentpestattacks[24–26].Amajoradvantageof
Box1.Definitions
TheConceptofIPM
Aholistic‘approach’or‘strategy’tocombatplantpestsanddiseasesusingallavailablemethods,whileminimizing
applicationsofchemicalpesticides.
TheScienceofIPM
Thesystematicstudyofthecompatibilityandoptimizationofsimultaneouslyimplementedactionsassociatedwithat
primingisthat thedefenses are notturned onuntil needed,thus reducingthe associated metaboliccosts.Innature,primingand/ordefensescanbeinducedbyvariousbioticorabiotic factors,includingherbivore-inducedplantvolatiles[27],eggdeposition[28],heavymetalstress
[29],andsoilmicrobes[30].OneinterestingopportunitydiscussedbyPinedaetal.[30]isto transplant‘healthysoil’withbeneficialmicrobesforprimingorinducingdefensesofcropplants. KeyFigure
The
Integrated
Pest
Management
(IPM)
Pyramid
Showing
the
Most
Important
Pest
Management
Elements
Biological control In te a n d in tr a -specific bot anic al div e rsity Intrinsic herit able pl an t r esis tance Chemical pescides
Mechanical, physical, cultural, opc, and audave control
Plan t vac cina on Bior a onal s yn the c vo la les
Figure1.ThebasetieroftheIPMpyramidconsistsofabioticactionsthatcanbeappliedbeforeorimmediatelyafter
plantingandmaycontinueuntilharvesting.Thenfollowsacirculartierconsistingofimportantelementsthatcanbe
classifiedas‘ecological’andformthebasisforecology-basedIPM.Finally,thetoptierofthepyramidincludeschemical
pesticidesthatshouldonlybeappliedwhennecessary,ifthemorebasalIPMelementsfailtokeeppestpopulationsunder
theeconomicthreshold.Arrowsdenoteparticularlyimportantinteractionsbetweentheecologicalelements.Theseseven
Inothercases,seedsorplantscanbetreatedbeforesowingorplanting,thusprovidingthe growerwithresistantmaterialfromdayone.Forexample,tomatoplantsgrownfrom jasm-onate-andb-aminobutyricacid-treatedseedsreportedlyhavestrongerinduceddefensesthan controlsagainstbotharthropodpestsandpathogenicfungi[31].Challengesforfutureresearch includethedevelopmentoftechniquesthatprovidedefensesagainstseveralpests simulta-neouslyand improvethe consistency of primingresponses.To meetthis objective, better understandingofthemolecularmechanismsinvolvedinprimingdefensestotargetedpestsis required.
Inter-andIntra-SpecificBotanicalDiversity
Theimportanceofbiodiversityforecologicalprocessescanhardlybeoverstated[32,33].Inter alia,monoculturesarehighlysensitivetopestsandoftenseverelydamagedbyoutbreaks[34]. Thereareseveralreasonsforthissensitivity.Thefirstislackofintraspecificbotanicalvariation:a geneticmonoculturehasnovariationinresistancegenes,soallplantsinitwillbepotentially susceptibletoanypestcapableofestablishingacolonyinorononeofthem.Thus,resistance canbesignificantlyimprovedsimplybyusingseveralvarietiesinafield.Forexample,increasing thegenotypicbiodiversityofriceinChinahasreducedfrequenciesofriceblastby94%and increased yields by 89%, relative to those of genetic monocultures [35]. Accordingly,the temptationtouseasinglecultivarbecauseithashighpestresistanceiscounterproductive– mixturesalmostalwaysprovidehighercroppingsecuritythansinglecultivars,evenwhenthey includecultivarswithlowresistance[36].
Anotherreasonformonoculture’spestsensitivityistheirlackofinterspecificbotanicaldiversity: single-cropsystemsdonotbenefitfromany‘associationalresistance’[37]–thatis,reductionin plants’detectabilityby,andvulnerabilityto,pestslinkedtogrowthincommunitieswithother plantspecies.Althoughinterspecificdiversitypersemayreducepestproblems,theeffectcan begreatlyimprovedbyconsciouslycombiningplantspecieswithattractingandrepellingtraits. The‘push–pull’concept(whichcombinesuseofarepellantplantaroundacropanda‘trap crop’somedistancefromit)istodatethemostsuccessfulapproachtoprotectcropsfrom arthropodpestsusinginterspecificbotanicaldiversity[38].
Although a convincing body of literature shows that increases in inter- and intra-specific botanicaldiversityreducepestproblems,itisstillunclearwhichofthesetwofactorsismost important,andshouldbeprioritized.
BiorationalSyntheticVolatiles
Adevelopingpestcontrolstrategyistouse‘biorational’substances,whichhavelowtoxicityto nontargettaxaandincludevariousvolatilessuchasinsectpheromones[39]andplantvolatiles
[40](orderivativesofthesecompounds)thatinfluencepests’behavior.Todate,sex pher-omoneshavebeenthe mostfrequentlyapplied,oftenineffortsto disruptmatingofinsect pests. Thisinvolvesdispensing relativelylarge amountsofsex pheromonesin plantations, therebysuppressingmales’abilitiestofindfemaleconspecificsformating[39].Adisadvantage ofmatingdisruptionisthatitcannotbeusedcuratively.However,itisefficient,environmentally friendly,andrelativelyinexpensive.Otherimportantusesofpheromonesincludemasstrapping
[41]witheithermale-orfemale-producedpheromones,andherbivorerepellenceusingalarm pheromones[42].However,recentfindingsindicatethepresenceofrelativelyhighintraspecific variation in pheromone blends among pest populations [43]. Thus, further study of the populationspecificityof lures’efficacy,andthefeasibility ofdevelopingpheromoneblends forlocalpopulations,isrequired.Syntheticplantvolatileshavebeenusedlessextensively,and usuallyaspartsofpush–pullsystems[40,44].However,recentresearchsuggeststhatplant volatilessignificantlyinfluencethestrengthofinsectherbivores’responsestopheromones[45]. Thus,futureuseofplantvolatilesmaybemostsignificantaspartofblendswithpheromones.
BiologicalControl
Biologicalcontrol,orbiocontrol,istheuseoflivingorganismstoreducethepopulationdensity or impact of pests[46,47]. It is one of the oldest nonchemical control methods used in agriculture[47].Arthropodsaremainlycontrolledusingpredators,parasitoids,andpathogens, whileplantpathogensaremainlycombatedusingantagonisticmicrobes.Oftenviewedasthe cornerstoneofIPM,biologicalcontrolisprobablythemostwell-researchedelementoftheIPM concept,androotofsomeofthemostinnovativepracticalapplications.Forexample,‘flying doctors’(inoculatedbees)arebeingusedasvectorsforhigh-precisionapplicationsofmicrobial biologicalcontrolagentstofloweringcropsinfectedwithpathogenicfungi[48].Similarly,for20 years insecticidal proteins associated with the bacterial biological control agent Bacillus thuringiensishavebeenexpressedbytransformedBtcrops[49].
Mostoftheintrinsicproblemsassociatedwithbiologicalcontrolappearmainlyinopenareas witharthropodagents,whichinsomecasescanemigratefromtheplantationleavingthepest behind, attackeach other (intraguild predation) ratherthan the target pest [50],or attack nontargetprey[51].Aproblemmainlyassociatedwithmicrobialagentsisthatpestscanevolve resistance[52,53]. As we will see, some of these problems can be solved by combining biologicalcontrolwithactionsassociatedwithotherIPMelements.
IPMResearch:StrategiesforIntegrating theElements
AstheobjectiveofIPMistooptimizecombinedeffectsofactionsassociatedwiththeelements reviewedabove,thescienceofIPMshouldelucidateinteractionsbetweentheseactionsand formulatestrategiestooptimizetheinteractions’synergy(Figure1).Sevensuchinteractions (research areas; described below) are identified in this paper, and visualized in Figure 1. ParticularlyimportantresearchquestionsarepresentedintheOutstandingQuestionssection.
OptimizationofIntrinsicHeritablePlantResistanceforIPM
InteractionswithPlantVaccination
Ingeneral,effectsofprimingandinductionarestronglydependentonplantgenotype[54].For example,Hordeeaegrassessuchaswheat,barley,rye,andoatscanbevaccinatedagainsta rangeofherbivoresusingEpichloëmicrobesviaalkaloidalsecondarymetabolites[55]. How-ever,effectsofEpichloëmaybeeitherpositiveornegative,dependingonplantgenotype[55]. Thesefindingsprovidebreederswithnewopportunitiestooptimizeeffectsofplantvaccination, but show that neglect of this issue at the breeding stage may severely impair results of vaccination.Thepaucityofknowledgeabout andguidelinesfor breedingto facilitateplant vaccinationagainstpestsconstitutesamajorobstacle,whichwillrequireinvestmentsinbasic molecularresearch.Onthemorepositiveside,newgeneticresourcesfromwildcroprelatives, andnovelgenomeeditingtechnologies,providehopeforprogressinthisarea.
InteractionswithBiorationalSyntheticVolatiles
Recentresearch hasshown that defensiveplant semiochemicals can makeherbivoresex pheromones either less or more attractive to conspecifics. More specifically, herbivorous cotton leafworms are only reportedly attracted to mating sites by sex pheromones inthe presenceofcertaincombinationsofhostvolatiles,andsingleplantdefensecompounds(such as4,8-dimethylnona-1,3,7-triene)can stronglysuppress pheromonesignals[45,56].These discoveriesopenupnewopportunitiesforbreederstomodulateplants’profilesofvolatilesthat interactwithsex pheromones,thereby signaling to herbivoresthat a crop plantationisan unsuitablematingsiteorfacilitatingmasstrappingwithpheromonetraps.Realizationofthese possibilitieswillrequiremoreknowledgeofinteractionsbetweenplantvolatilesandpheromone signals, andthus newcreative collaborations betweencrop breeders andinsect chemical ecologists.Futureattemptstotransformcropstoreleasepestalarmpheromones[57]mayalso
benefitfromconsideringplantsemiochemicals,asoverallpheromoneandplantvolatileprofiles maybetheultimatedeterminantsofpestbehavior.
InteractionswithBiologicalControl
Intrinsicheritable plant resistance affects notonly pests butalso beneficial organisms like biologicalcontrolagents.Forexample,predatorybugsusedforbiologicalcontroloftensuck plantsap,ornectarwhosequalityaffectstheperformanceandbiologicalcontrolefficacyofthe predators[19,58,59]. By contrast,parasitoids are exposed to the plant material thattheir herbivoroushostsconsume,andarethusindirectlyaffectedbyplant-resistancetraits[16,60]. Inaddition,physicalplantdefensessuchastrichomesareknowntoaffectbiologicalcontrol agents[11].Whiletheseexamplesshowthatplanttraitsaffectbiologicalcontrolagents,itisstill largelyunknownhowplant resistanceultimately affectsplant damageinthe presenceand absenceofbiologicalcontrol[61,62].Predators,parasitoids,andpathogensmaybedifferently affectedbydifferentkindsofplant-resistancetraits,allowingcropbreederstodesigncultivars suitableforspecificbiologicalcontrolagents[62].
Plantvolatilestoocouldbeusedtoimprovebiologicalcontrol,andabreedingstrategyforthis purpose has been published elsewhere [19]. However, important problems remain to be solved.Forexample,attractionofbiologicalcontrolagentstovolatile-emittingcropsstillworks bestatsmallscales[63].Tomakeindirectdefensesmorerelevant,weneedtounderstandhow toattract(andretain)sufficientnumbersofbiologicalcontrolagentsto,forexample,largemaize fields.
OptimizationofPlantVaccinationforIPM
InteractionswithBiologicalControl
ResearchonplantvaccinationinIPMcontextsislimited[64].Apotentialriskisthatwhenbasal plantdefensesareinducedorprimed,notonlypestsbutalsobeneficialorganisms,liketheir predators,willalsobeexposedtothedefenses[65].However,inthefewstudiesthathave investigatedeffectsofplantvaccinationonpredation,positiveeffectsonpredationrateshave been detected. For example, induction of cotton defenses can induce omnivorousthrips (Frankliniellaoccidentalis)to switchfrom feedingonhost cottonplantsas peststo feeding onherbivorousspidermiteeggs[66].Inaddition,tworecentstudiesfoundthatplant-feeding predatorscanbeusedto vaccinateplants,as thepredatorybug Macrolophuspygmaeus, whichisoftenusedasabiologicalcontrolagent,caninduceproteinaseinhibitor(PI)activityand accumulation of transcripts of the PI-II gene in tomato [67], consequently reducing pest pressure [68]. Thus, some biological control agents could theoretically be introduced to plantletsinnurseriesforvaccinationandthenhitch-hikewiththeplantstothefinalgrowing areas to provide biological control services. Apart from these intriguing results, possible synergies between plant vaccination and biological control have been almost completely unexplored,andarewideopenfornewidea-basedresearch.
OptimizationofInter-andIntra-SpecificBotanicalDiversityforIPM
InteractionswithBiologicalControl
AfavoritetopicformanyIPMresearchersistheoptimizationofplantdiversityforbiological control.Todate,thisisprobablythemostintensivelyinvestigatedareaofIPM,havingproduced importantpracticalapplicationssuchasintercropping[69],flowerstrips[70],andvarioustypes ofhabitatmanagement[71].TheideabehindthisIPMapproachistoaddplant-basedfood, shelter,andalternativepreytobiologicalcontrolagents,whilemaintainingthedirect associ-ationalresistancetopestsasdescribedearlier.Functionalbotanicaldiversityisoftenobtained byaddingcompanionplantscarryingfloralorextra-floralnectar[19].Forexample,arecent multicountrymultiyearstudyshowedthatplantingnectar-producingplantsaroundricefields increasedtheabundanceofpredatorsandparasitoids,whilepestpopulationswerereduced
[72].Interpretingresultsofthesestudiesisnotstraightforward,partlybecausegenerallytheydo not show causal relationships (only correlations) between increases in botanical diversity, improvementsinbiologicalcontrol,andreductionsinpestdensities.Thus,thereisoftenonly speculativeunderstandingofthemechanismsresponsibleforthebeneficialeffects.Inaddition, interventionsatverylocalscales(e.g.,mixedintercropping)[73]tolandscapescales[74]can reportedlyhavebeneficialhabitateffects,butfurtherresearchisneededtoidentifytheoptimal spatialscaleofbotanicaldiversificationtofavorbiologicalcontrolagents[71].Asyet,almostall IPMresearchregardingeffectsofbotanicaldiversityonbiologicalcontrolhassolelyfocusedon interspecificdiversity.However,botanicaldiversitycouldalsobemanipulatedattheplanttrait
[75]orplant genotypiclevel[76–78].Themechanisms wherebyintraspecificplant diversity affectsbiological controlagents areunknown, butcouldinvolve effects onpests[78]. For example,variationinpestdevelopmenttime,whichcanbeenhancedbymixingresistantand susceptiblecultivars,cansuppresspredator–preycyclesandmitigatepestoutbreaks[79].To date,interspecificandintraspecificcropdiversityhasnotbeensimultaneouslymanipulatedin anypublishedstudy, leavingabundant opportunitiesforfutureIPMresearchto explorethe optimaltaxonomiclevel(s)ofdiversity.
OptimizationofBiorationalSyntheticVolatilesforIPM
InteractionswithBiologicalControl
Although pheromones presumably evolved because of their ability to trigger behavioral responsesinconspecifics,theycan sometimesbeexploitedbyotherorganisms[80,81].If predatorsandparasitoidsuseherbivorepheromonestolocatetheirprey[82],massreleaseof sex pheromones to disrupt mating could also disrupt biological control. However, most predatorsandparasitoidstendtotargetimmaturestagesoftheirprey(eithereggsorlarvae), whichdonotproducesexpheromones.Thus,inmostcasesbiologicalcontrolofherbivoreswill notbe affectedby the use of synthetic sexpheromones, but the possible utility of other herbivorepheromonesinbiologicalcontrolmeasuresshouldbefurtherexplored.Forexample, aphidalarmpheromones[80]havetwoknownbiologicaleffects:(i)disruptingaphidfeedingon theirhostplants,and(ii)actingaskairomones,attractingnaturalenemiesoftheaphids[57,83]. Thus,transformingcropstoreleaseaphidalarmhormonesisapromisingstrategy.Inarecent study,theparasitoidAphidiuservispentmoretimeforagingonahexaploidvarietyofwheat followingtransformation oftheplant,enablingit toreleasetheaphid alarmpheromone
(E)-b-farnesene[57],butthisdidnotsuppressaphidinfestationsinthefield.Acomplicatingfactor isthataphidalarmpheromonesareconsideredshort-rangecuesagents[84],whichmayhave littleabilitytoattractnaturalenemiesfrom faraway.However,combiningpheromoneswith plantvolatiles, whichoftenhave longerranges,may bean effectivestrategy. Furthermore, predatorsandparasitoids can quicklylearnto disregard dishonest signals[85]. Therefore, futureresearchshouldinvestigatethepossibilitiestoreleaseaphidalarmpheromonessolely afteraphidattack,toguidepredatorsandparasitoidsspecificallytodamagedplants.
OptimizationofBiologicalControlforIPM
InteractionswithIntrinsicHeritablePlantResistance
A major problem in modern agriculture is that pests rapidly evolve counter-resistance to previouslyresistant cultivars [86–88]. Recent research suggeststhat crop breeders’ arms raceswithpestscanbesupportedbybiologicalcontrolagents[89].Thetheoretical back-groundforbiologicalcontrol-aideddurableresistancewaslaidoutalready25yearsagowhen Gouldetal.[90]suggestedthatbiologicalcontrolagentsthatdecreasethedifferentialpest fitness between resistant and susceptible cultivars should delay the evolutionof counter-resistanceinthepest.ThishypothesiswastestedinexperimentswithBtbroccoliexpressing Cry1Ac,herbivorousdiamondbackmoths,andpredatoryladybeetles[89].Aspredicted,the herbivoreevolvedcounter-resistancetoBtbroccolimuchmoreslowlyinthepresenceoflady beetles.
Thepossibilitiesto increase thedurabilityof crop resistanceto pestsbyapplying inherent resistance-enhancingmeasuresincombinationwithbiologicalcontrolareintriguing,buthave receivedfartoolittleattentionbyIPMresearchers.Bothevolutionarymodelingand manipula-tiveexperimentsareneededtoincreaseourunderstandingoftheinteractionsinvolved,andthe circumstancesneededtoprolongresistanceviabiologicalcontrol.
ConcludingRemarksandFuturePerspectives
Holistic IPM involving all action levels is probably unattainable, and we are currently not anywherenearobtainingcompleteandoptimalprogramsforresearchorapplications. How-ever,greatprogresscanbemadeifthesevenresearchareasoutlinedaboveareprioritized. Mostpreviousecology-basedIPMresearchhasfocusedonintegratingbotanicaldiversitywith biological control,while measures intended to enhance plant resistance, vaccination, and pheromone-basedmanipulationshavebeenmainlytreated(ifconsidered atall)as noninte-gratedsupplements.Whileintegratingdiversity/biocontrolisveryimportant,mostoftheseven classesofIPMinteractionsclearlyinvolveeffectsof,oron,plantresistance.Thus,thereare manyunexploredopportunitiesto improveIPMthroughbreeding,butalso numerous chal-lenges.IPMresearchershavepaidrelativelylittleattentiontotherolesofplantgeneticsasyet, butthismustchangeifIPMisto reach itsfullpotential.Plantbreeders,inturn, shouldbe encouragedtoparticipateinfutureIPMprogramstoagreaterdegree.Theoptimalsolutionmay notalwaysbetomaximizeplantresistance,buttooptimizeitfromaholisticIPMperspective. BreedersshouldbenefitfromtheIPMframework,because (forexample)efficientbiological controlcanhelptoenhancethedurabilityofplantresistancebyweakeningnaturalselectionfor counter-resistanceinpests[89,90].Furthermore,duetothedependenceofeffectsofactions atotherlevelsonplantbreedingprograms,breedersinevitablybearhighresponsibilityforthe outcomeofIPMprograms,andmustconsiderthesuitabilityoftheircultivarswithinprevailing IPMframeworks. Asplant resistanceaffects phenomena associated withmost other IPM elements,inmanycasesmathematicalmodelingwillberequiredtoidentifytheoptimallevelof resistance.Recent modeling to elucidate the optimal resistance for biological control ina systemconsisting ofa hostplant, aspecialist herbivore,and anomnivorouspredator has demonstratedtheutilityoftheapproachformanagingthecomplexityofIPM[58].
Aburningissueis whetherornottoaccepttransformedplantsinIPMprograms.Previous studiesoftendismissedtheuseofgeneticallymodified(GM)crops[91],whileamorerecent paperclearlystatesaperceivedneedtoapplymodernbreedingtechniques[92].Breedingto realizecomplexIPMsolutions,ofteninvolvingcombinationsofseveralplantresistancetraits, willbealmostimpossibleusing onlyclassical breedingtechniques. Thus,parts ofthe IPM communitymayneedto adjusttheirideologyto achievefunctionalandsustainableholistic solutions.
AnotherconclusionthatcanbedrawnfromtheIPMpyramidisthatbiologicalcontrolisthe mostsensitiveelementtoactionsatotherlevels.Whateverisdonetocombatpestswillalmost certainlyalso affectany biologicalcontrolagents. Thisoffersabundant potentiallyvaluable opportunities fornovel synergistic measuresas the effects ofmodulating plant resistance, vaccination,andpheromonetreatmentsonbiologicalcontrolhavereceivedparticularlylittle attention. In these contexts, mathematical modeling will also likely play important roles in elucidatingoptimalsolutionsasitwillbefrequentlytoodifficult,orexpensive,toconstruct full-factorialexperimentscoveringallrelevantIPMelements.
Asmanynationalandintergovernmentalbodieshavealreadyformulatedregulations prescrib-ingIPM[1],theresearchcommunityhasamajorresponsibilitytoaddressthecomplexscientific problemsthatmustberesolvedtorealizeitsfullpotential.Integrationofactionsatallofthe
OutstandingQuestions Intrinsicheritableplantresistance
(i)Integrationwith‘plantvaccination’
Whichplantgenes,traits,and
mecha-nismsenablesomeplantgenotypesto
respondstronglytopriming/induction
stimuli,whileothersrespondweakly?
(ii) Integration with ‘biorational
syn-theticvolatiles’
Whichplant semiochemicalmixtures
andsinglecompoundsinterferewith
herbivore pheromone signals? Can
plantsbetransformedtorelease
opti-malblendsofherbivorepheromones
andsemiochemicals?
(iii)Integrationwith‘biologicalcontrol’
Whichdirectandindirectplant
resis-tancetraitsaffecttheperformanceand
efficiencyofbiologicalcontrolagents?
Do predators, parasitoids, and
microbesresponddifferentlytofocal
planttraits?
Plantvaccination
(iv)Integrationwith‘biologicalcontrol’
Doesplantvaccinationaffectthe
per-formanceandefficiencyofbiological
controlagents?Towhatextentcan
biologicalcontrolagentsbe usedto
vaccinateplants?
Inter-andintra-specificbotanical diversity
(v)Integrationwith‘biologicalcontrol’
Whatare the optimal temporal and
spatialscalestomanipulatebotanical
diversity to favor biological control?
Whichplanttraitsmediatefunctional
diversity? What is the optimal level
(trait,species,orcultivar)tomanipulate
botanicaldiversitytofavor biological
control?
Biorationalsyntheticvolatiles
(vi)Integrationwith‘biologicalcontrol’
Towhatextentcanbiologicalcontrol
agentsexploitdifferentkindsofpest
pheromones? Can the attraction of
naturalenemiesfromadistanceusing
alarm pheromones be improved by
addingplant semiochemicals to the
volatileblend?
Biologicalcontrol
(vii)Integrationwith‘intrinsicheritable
elementswithintheecologicaldomainwillrequireintenseassiduousbasicresearch,butwill probablyprovidenumerousstrongsynergisticeffects thatwill increase thesustainabilityof agriculture.Recentbreakthroughshighlightingimportanteffectsofplantresistancetraitson pheromonesignaling[45]andbiologicalcontrolagentsonplantvaccinationresponses[67,68]
arejusttwoexamplesshowingthatnewscientificunderstandingislayingfoundationsforrapid advancesinIPM.ThenewscienceofIPMhastheintrinsiccapacitytoenableefficientand sustainablefoodproductionto feedtheworld’s increasingpopulation,andreplace alarge proportionofcurrentlyusedtoxicpesticides.Theproposedconceptualframeworkisintended toassisteffortstorealizethisvision.
Acknowledgments
StenbergisfundedbyTheSwedishResearchCouncilFormas(GrantNos.217-2014-541and216-00223),TheCrafoord
Foundation(GrantNos.20150904and20161057),andCarlTryggersStiftelse(GrantNo.CTS15:468).
SupplementalInformation
Supplementalinformationassociatedwiththisarticlecanbefound,intheonlineversion,athttp://dx.doi.org/10.1016/j.
tplants.2017.06.010.
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