《生物入侵》发表论文(英文)

BiolInvasions(2012)14:649–658DOI10.1007/s10530-011-0106-8

ORIGINALPAPER

Historyofexposuretoherbivoresincreasesthecompensatoryabilityofaninvasiveplant

XinminLu JianqingDing

Received:21December2009/Accepted:14September2011/Publishedonline:25September2011ÓSpringerScience+BusinessMediaB.V.2011

AbstractReleasefromnaturalenemiesisfrequentlycitedasanimportantfactorcontributingtoplantinvasions.Butsucheffectsarelikelytobetempo-rary—nativeherbivorescanformnewplant-herbivoreassociationsandco-evolvedinsectsmightreachthenewrange.Whilethepotentialeffectsoftheinitialenemyreleasehavebeenwellstudied,theconse-quencesofanyresumptionofherbivoryarepoorlyunderstood.AlternantheraphiloxeroidesisoneofthemostwidespreadinvasiveplantsinChinaandisattackedbothbyaspecialistherbivoreintroducedfromthenativerange,Agasicleshygrophila,andanativebeetleCassidapiperataHopewhichhasformedanewassociation.However,theseinsectsarenotfoundthroughouttheinvadedrange.Totesttheeffectofthehistoryofpopulationexposuretoherbivoryoncompensatoryability,plantswereculturedfrom14populationsaroundChinathatdifferedinwhetherA.hygrophilaorC.piperatawerepresent.TreatmentplantswereexposedtoherbivorybyA.hygrophilaforaweekuntil50%oftheleafareawasdefoliated,thengrownfor80days.Plantsfrompopulationswithpriorexposuretoherbivory(ofanykind)accumulatedmore

rootmassthanpopulationswithoutpriorexposure,indicatingthatpriorexposuretoinsectscanstimulateplantcompensationtoherbivory.Wewouldrecom-mendthatpotentialchangesinplanttoleranceinresponsetopriorexposuretoherbivoryareconsideredininvasiveplantmanagementplansthatemploybio-controlagents.

KeywordsBiologicalcontrolÁBiologicalinvasionÁInsectexposurehistoryÁAlternantheraphiloxeroidesÁCompensation

Introduction

Mostinvasiveplantspecieshavebeenintroducedtotheirnewrangeswithoutthefullsuiteofnaturalenemieswithwhichtheyco-evolved(e.g.naturalenemyrelease)(KeaneandCrawley2002).Intheabsenceofspecialistherbivores,invasivespeciesmayreallocateresourcesfromdefencetogrowth,repro-ductionorboth,asproposedbytheEvolutionofIncreasedCompetitiveAbilityHypothesis(EICA)

¨tzold1995).However,theenemy(BlosseyandNo

release,andtheassociated tnessgain,mightbetemporaryasnativeherbivorestendtoaccumulateonnon-nativespeciesovertime(Siemannetal.2006).Moreover,co-evolvednaturalenemies,suchasher-bivorousinsects,mightalsoeventuallyarriveeitheraccidentallyordeliberately(e.g.throughclassicalbiologicalcontrolreleases),althoughthecharacterand

X.LuÁJ.Ding(&)

KeyLaboratoryofAquaticBotanyandWatershedEcology,WuhanBotanicalInstitute/WuhanBotanicalGarden,ChineseAcademyofSciences,Wuhan,Hubei430074,Chinae-mail:ding@

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650intensityofthere-associationbetweenplantandherbivorecandifferfromtheinteractioninthenativerange(Garcia-Rossietal.2003).

Inresponsetothere-ornew-associatedinteractionswithherbivores,invasiveplantsmayundergorapidevolutionarychangesindefence,e.g.resistanceand/ortolerance(Thompson1998).Forinstance,inpopula-tionsofinvasivewildparsnips,Pastinacasativa,therewasanincreaseintoxicfuranocoumarinscontentafterre-associationwithParsnipwebworm,Depressariapastinacella(ZangerlandBerenbaum2005),leadingtoanincreaseinherbivoreresistance.Whathasreceivedlessattentionisthepotentialforinvasiveplantstoevolvegreatertoleranceofherbivoryafterre-ornew-associationwithherbivores.

Toleranceistheabilityofaplanttore-growandreproduceafterherbivory(StraussandAgrawal1999).Plantcompensatoryability,de nedhereasthedifferencein tnessbetweenherbivorydamagedandundamagedindividualsofthesamegenotype,isknownasanimportantmeasureofplanttolerance(Belsky1986).Herbivory-inducedcompensatorygrowthforasingleplantgenotypecanrangefromunder-compensationifherbivorydamageisnotfullyreplaced,toequal-compensationifplantsfullyrecoverfromherbivory,andovercompensationifplantshavegreater tnesswhendamaged(MaschinskiandWhitham1989).Proposedmechanismsforplantcompensationincludeincreasesinphotosyntheticability,utilizationofstoredreserves,andchangesinphenologyandresourcereallocation(StraussandAgrawal1999;Tif n2000).Empiricalevidenceindicatesthatherbivorymayevolutionarilyincreaseaplant’scompensatoryability,especiallywhentheriskofdamageispredictableandhigh(JuengerandBergelson2000;Lennartssonetal.1997).Therefore,there-ornew-associatedherbivoreswouldbeexpectedtocreateaselectionpressureonthecompensatoryabilityofinvasiveplants,particularifherbivoresoccurathighdensities.

Theevolutionaryresponsesofinvasiveplantsto

herbivorehavebeenwellstudied(Mu

¨ller-Scha¨reretal.2004),providinginsightsintomanyaspectsofplantevolutionarybiology,especiallyevolutionof

plantdefence(Mu

¨ller-Scha¨reretal.2004;Thompson1998).However,almostallthesestudiesfocusonsexualplants,whilelittleinformationisavailableontheevolutionaryresponsesofclonallypropagatedinvasiveplantstoherbivores.Infact,someofthe

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globallyimportantinvasiveplantsreproducemainlyclonally,e.g.Alternantheraphiloxeroides(Julienetal.1992)andEichhorniacrassipes(Lietal.2006),intheirnon-nativeranges.Thereisincreasingevidenceindicatingthatsomaticmutationandgenomicmodi- cationinclonalplantsarefrequentandprovidegeneticandepigeneticvariationthatcontributestotheiradaptiveevolution,especiallyforclonallyprop-agateddomesticatedplants(Prentisetal.2008;McKeyetal.2010).Moreover,intra-clonalvariationinplantdefenceandselectiveimpactsofherbivoryonplantdefencehasbeenreportedinclonalplants(MonroandPoore2004;WhithamandSlobodchikoff1981).Therefore,herbivorycanimposeselectionondefenceofclonalinvasiveplants;indeedsucheffectsarelikelytobepromotedbytheinvasionprocess(Prentisetal.2008).

Here,wereporttheresultsofanexperimentdesignedtoexaminetheconsequencesofpriorexposuretoinsectherbivoresonthecompensatoryabilityoftheclonalinvasiveplantalligatorweed,Alternantheraphiloxeroides(Mart.)Griseb(Ama-ranthaceae).Speci cally,wehypothesizedthatplantpopulationsfromsiteswithherbivoreswouldshowagreatercapacityforcompensationthanpopulationsfromsiteswithoutthem.Wealsotestedwhetherthesourceofherbivoryencountered(nativeinsects,introducedinsects,orboth)in uencedtheformofplantcompensation.

MaterialsandmethodsStudyspecies

Alternantheraphiloxeroidesisaperennialherbaceousplantwithhorizontaltoverticalstemsthatcangrowinaquaticandterrestrialhabitats.Eachstemconsistsofnodesthatarecapableofproducingindividualplant-lets.Rootsdevelopatcloselyspacednodesalongstems(Julienetal.1995).ThespeciesisnativetoSouthAmericaandhasbecomeawidespreadinvaderintheAsia–Paci cregionandtheUnitedStates(Julienetal.1995).Itwas rstintroducedintoChina(Shanghai)asaforageplantinthe1930s,andsincethenithasbeendistributedtoasmanyas20provincesinCentralandSouthernChina(Ma2001),withitsrangestillexpandinginNorthernChina(Gengetal.2007).AccordingtoJulienetal.(1992)A.philoxeroides

Insectexposurehistoryincreasesaninvader’scompensatoryability651

producesseedsinitsnativeSouthAmericanrange,butrarelysetsseedsandpropagatessolelybyvegetativemeansfromstemandrootbudsinAustralia,theUnitedStatesandChina.

Agasicleshygrophila,ahost-speci cleafgrazerofA.philoxeroides,hasbeenwidelydistributedforbiologicalcontrol(Buckingham2002).ThebeetlehascurbedA.philoxeroidesinvasioninmanyinfestedriversandponds(Ma2001;Saintyetal.1998),buthasfailedtocontroltheplantinsemi-aquaticandterres-trialhabitatsdespiteoccurringonA.philoxeroidesinthesehabitats(Ma2001).Thebeetlewas rstintro-ducedtoChinain1986,buthasnotspreadtoallareasaffectedbyA.philoxeroides(Ma2001),andsoplantpopulationshavedifferenthistoriesofre-association.InChinaA.philoxeroidesisalsodefoliatedbyanativetortoisebeetle,CassidapiperataHope(Coleoptera:Cassididae)(Linetal.1990)interrestrialhabitatsandoccasionallyinaquatichabitats(LuandDing,unpub-lished).BothA.hygrophilaandC.piperataareabovegroundherbivores.AdultsandlarvaeofA.hygrophilafeedonleavesandstemsofA.philoxe-roides,oftenproducingfeedingholesand‘‘trenches’’onleaves;adultsandlarvaeofC.piperataonlyfeedonleavesofA.philoxeroides,oftenproducingtinyfeedingholes.PreviousstudieshavefoundthatA.philoxeroidescancompensaterapidlyintermsofbiomassproductionafterdamagebyherbivory(naturalandsimulated)andmowinginterrestrialhabitats,whichmayberelatedtoitshighrootmass(Luetal.2010;LuandDing2010;Sunetal.2009;Wilsonetal.2007).Moreover,incommongardenexperimentswefoundthatA.philoxeroidescompensatesfordefolia-tioncausedbyA.hygrophilaandC.piperatainasimilarmanner(LuandDing,unpublished).

Inthisstudy,wefocusedonherbivorybyA.hygrophila.TheA.hygrophilaadultbeetlesusedinourexperimentswerecollectedfromA.philoxero-idesinthesuburbsofWuhan,HubeiProvince.Plantsamplinglocations

Inearlyspring2007,wecollectedplantsfrom14terrestrialpopulations([10kmapartfromeachother)ofA.philoxeroidesin veChineseprovinces(Table1);populationsfromthesameprovincewereassumedtobeindependentforpurposesofthisstudy.Basedonbiologicalcontrolrecords(Ma2001;Yang2001),feedingrecordsforC.piperata(Linetal.

1990),andour2006–2007 eldsurveysoninsectfeeding,thesepopulationswerecategorizedintofourgroupsbasedonthepresence(orabsence)ofA.hygrophilaandC.piperata(Table1).Ateachsitewecollected10plantsfrom4locations(40plants/population)[20mapartinopen eldsnearaquatichabitats(riverbank).Wecollectedastem(10–15cmlong)fromeachplantandimmediatelyplacedthestemsinmoistfoamincoolerswithdryicefortransporttothelaboratory.Inthelaboratorywecutstemsto4–5cmlengths;eachcutstemcontainedasinglenode.Stempieceswerethenplantedverticallyinplasticcontainers(50940930cmdeep) lledwithahomogenizedmixtureofpeat,topsoilandsandinagreenhouseundernaturallightatWuhanBotan-icalGarden(ChineseAcademyofSciences).Thecontainerswerecagedtoexcludeherbivores.Toreducethepossiblecarryoverimpactofparentalenvironmentonplantcompensation,weremoved4–5cmstempieces(eachbearingonenode)fromthenewshootsforourexperimentsafter10weeks.

Herbivorytreatments

TheexperimentwasconductedinagreenhouseatWuhanBotanicalInstitute/WuhanBotanicalGarden(ChineseAcademyofSciences)fromApriltoearlyDecember,2007.Meandailyairtemperatureinthegreenhousewas20–35°CfromlateApriltoSeptemberand15–25°CfromOctobertoearlyDecember.

Threerandomlyselectedstempiecesfromthesamepopulation(stemsfromthesamepopulationweremixedtogetherbeforeplanting)wereplantedverti-callyinapot(16cmindiameter,14cminheight) lledwithahomogenizedmixtureofpeat,topsoilandsand.Twentydaysbeforeherbivorytreatment,weretainedsimilar-sizedplantsandthinnedtheplantstooneplantperpottominimiseplantsizevariationamongpots.Dependingontheavailabilityofstempieces,therewere34–46plantsperpopulation.

Halfthepottedplantsforeachpopulationreceivedinsects(herbivorytreatment:50%oftheleafareaofeachplantwasremovedbyherbivores),andhalfservedascontrols(undamagedcontrol)(giving17–23replicatesforeachtreatment).Twodaysbeforeherbivorytreatment,halftheshootsforeachplantwerecaged.Intheherbivorytreatment,6–8A.hygrophilaadultswerereleasedintoeachcage.

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652

Table1LocationsofsourcepopulationsofA.philoxeroidesandtheirinsectexposurehistoryProvinces/populationsYunnanHGKMDCDLShanghaiCMYSLHQNHLHLZhejiangLPHenanXYHubeiZWYYMCShandongSD

36°41040.300

116°54050.500

–

32°00054.90030°32044.50030°32032.300

114°05013.600114°24045.600114°18032.700

NI?N–

20–40%20–40%

1987

30°24023.500

120°18006.000

I?N

30–40%

1987

31°34023.00031°10047.20031°10029.70031°1004.431°0745.6

00

0000

X.Lu,J.Ding

LongitudeLatitude

ExposurehistoryDefoliationlevelReleasetime

Reference

24°58046.00024°58036.40024°57038.40025°4317.2

00

102°39057.900102°39058.800102°33027.700100°1131.0

00

II––N––IN

20–30%20–30%

19871987

Ma(2001)Ma(2001)

121°30021.700121°23022.600121°22032.400121°3420.0121°2339.6

00

0000

10–20%

10–20%20–30%

1995Yang(2001)

Ma(2001)

Ma(2001)

ExposurehistoryiscategorizedasexposuretoA.hygrophila(I),C.piperata(N),both(I?N)orneither(–),asjudgedfromrecordsofreleaseofA.hygrophila(citedunderReferenceinthetable)andfromsurveysin2006–2007.Defoliationlevelisfromthesesurveys.ReleasetimeisforintentionalreleaseofA.hygrophila

After7days,allthecagedshootsintheherbivorytreatmentwerecompletelydefoliatedandtheinsectsandcageswereremoved.Plantswerethengrownforanadditional80days.Duringthistime,plantswerewateredevery2daysandpotpositionsinthegreen-housewererandomisedeverymonth.Atharvestthenumbersofstemandrootbudswerecounted,andaboveandbelowgroundbiomasswereseparatedanddried(80°Cfor48h)beforeweighing.Dataanalysis

Priortoanalysis,total,rootandshootmass,androottoshootbiomassratio(R/S)werelog10-transformedtoachievenormalityandhomoscedasticity.

Wecarriedoutanalyseswiththefulldataset,includingdataforallharvestedplants,totestthepotentialimpactsofherbivory,insectexposurehistory(previouslyexposedorun-exposedtoherbivory),populationandtheirinteractionsonplantperfor-mance.Wealsoanalysedthedataforplantswithinsectexposurehistoryonly(previouslyexposedtoA.hygrophila,C.piperata,orboth),tocomparetheimpactsofpreviousexposuretodifferentinsectspeciesonplantresponsetosubsequentherbivory.Allmeasuredplanttraitswereanalysedwiththree-waynestedANOVAs.Withthefulldataset,theANOVAmodelincludedinsectexposurehistory(previouslyexposedorun-exposedtoherbivory)andherbivorytreatmentas xedfactors,andplantpopu-lationasarandomfactornestedwithininsectexposurehistory.Forthedataforplantswithinsectexposurehistoryalone,theANOVAmodelincludedinsectspecies(A.hygrophila,C.piperata,orboth)andherbivorytreatmentas xedfactors,andplantpopu-lationasarandomfactornestedwithininsectspecies.Theeffectsofinsectexposurehistoryandinsectspeciesweretestedoverthenestedpopulationterm.Differencesbetweenindividualmeansweretestedwithttests.

DataanalyseswerecarriedoutusingStatisticalanalysissystem(SASVersion8.1,SASInstitute).

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Insectexposurehistoryincreasesaninvader’scompensatoryability653

Results

EffectofherbivoryandinsectexposurehistoryonplantbiomassandvegetativebudformationTheinteractionbetweenherbivoryandinsectexpo-surehistoryaffectedplantrootmass,butdidnotaffectplantshootmass,R/S,ortotalbiomass(Table2,Fig.1).Insupportofourprediction,herbivorysignif-icantlyincreasedrootmass(P=0.0007,Fig.1c)ofplantswithinsectexposurehistorywhencomparedtoundamagedcontrolplants,whileherbivorydidnotaffectrootmassofplantswithoutinsectexposurehistorywhencomparedtoundamagedcontrolplants(P[0.05,Fig.1c).

Theinteractionbetweenherbivoryandpopulationhadasigni canteffectonplanttotalandshootmass,andmarginallyaffectedplantrootmass(Table2).Ofthe14plantpopulations, veovercompensated,eightequal-compensatedandoneunder-compensatedintermsofplanttotalbiomassinresponsetoherbivory(Fig.2a).Insupportofourprediction,fourofthe vepopulationsthatovercompensatedforherbivory(HG,XY,ZWYandLHL)werefromlocationswith

Table2Athree-waynestedANOVAfortheeffectsofinsectexposurehistory(Eh),population(P),herbivory(H)andtheirinteractionsonplanttotal,rootandshootmass;roottoshootSourceofvariation

df

TotalbiomassF

ExposurehistoryPopulation[Eh]HerbivoryEh*HP[Eh]*HError

Sourceofvariation

1,1212,4021,4021,1212,402402df

Totalno.ofbudsF

ExposurehistoryPopulation[Eh]HerbivoryEh*HP[Eh]*HError

1,1212,3991,3991,1212,399399

0.00019.0206.5300.4541.470

P0.99<0.00010.0110.510.13

0.05825.8105.0603.8193.030

P0.81<0.00010.0250.0750.0004

herbivoresthatremoved10–40%plantleafareahistorically,whileonlyone(YMC)wasfromalocationwithnoherbivoresandhadnoknownhistoryofherbivoreinteraction(Fig.1a,Table1),andtheone(DL)thatunder-compensatedforherbivorywasfromalocationwithnoknowninsectexposurehistory(Fig.2a).Inthreeoftheovercompensatingpopula-tions(HG,ZWYandYMC),theshootmassofdamagedplantswassigni cantlyhighercomparedwiththatoftheundamagedplants(Fig.2b).

Thetotalnumberofvegetativebudswasonlyaffectedbyherbivoryandplantpopulation(Table2),whichdidnotsupportourpredictions.Thetotalnumberofvegetativebudswasgreater(14.57%,F1,426=1.787,P=0.008)indamagedthanincontrolplants.Thenumberofrootbudswassigni cantlyaffectedbyherbivory,plantpopulationandtheirinteraction,whereasthenumberofrootbudswasnotaffectedbyotherfactorsortheirinteractions(Table2),whichalsofailedtosupportourprediction.ThenumberofrootbudsofplantsfromHG,CM,HQandZWYpopula-tionsincreasedunderherbivory,whileherbivorydidnotin uencethenumberofrootbudsofplantsfromotherpopulations(Fig.2c).Thenumberofstembuds

biomassratio(R/S);totalnumberofbuds;andnumbersofrootandstembuds

Shootmass

P0.89<0.00010.0020.0060.061

F0.120724.3101.2601.7042.880

P0.73<0.00010.260.220.0008

R/SF0.2176.0503.0002.2911.410

P0.65<0.00010.0840.160.16

RootmassF0.01915.009.47010.771.720

No.ofrootbudsF0.0727.3909.6401.6561.800

P0.79<0.00010.0020.220.047

No.ofstembudsF0.6212.3301.3302.0061.210

P0.450.0070.250.180.27

Squarebracketsindicatenestingofterms

Statisticallysigni cantvalues(P\0.05)areinbold

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654Fig.1Effectofherbivoryinthegreenhouseexperimentonatotal,bshootandcrootmassofplantsexposedorunexposedtoherbivoresinthe eld:meansacrosspopulations.Valuesaremeans±1SE(backtransformedforthetotal,shootandrootmass).Symbolsabovepairsofbarsshowprobability(ttest)thatthetwomeansdidnotdiffer:(nosymbol)[0.05;*0.01–0.05;**0.001–0.01;***\0.001

wasaffectedbyplantpopulationandwasnotaffectedbyotherfactorsortheirinteractions(Table2).Differentialeffectsofpreviousexposuretodifferentinsectspecies

Fortheplantswithinsectexposurehistory,insectspecies(previouslydamagedbynative,introduced,orbothinsects)didnotin uenceplanttotalbiomass,totalnumberofvegetativebuds,ornumbersofrootandstembuds(Table3).Noneofthetraitswereaffectedbytheinteractionbetweenherbivoryandinsectspecies,whileplanttotalbiomass,shootmass

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X.Lu,J.Ding

andR/Swereaffectedbytheinteractionbetweenherbivoryandplantpopulation(Table3).

Discussion

Compensatorygrowthcanpotentiallyfacilitateaplantinvasion(Schierenbecketal.1994;WilseyandPolley2006)andcouldbeafactorthathampersthebiologicalcontrolofexoticplants(Garcia-Rossietal.2003).However,thishasreceivedlittleattention(Bossdorf

etal.2005;Mu

¨ller-Scha¨reretal.2004).WeexaminedherethecompensatoryabilityofA.philoxeroidespopulationsacrossitslargenewrangeinChina.Ashypothesized,wefounddifferencesincompensatoryabilitybetweenplantswithandwithoutinsectexpo-surehistory.A.philoxeroidespopulationsfromloca-tionswithinsectexposurehistoryaccumulatedmorerootmassandshowedgreatercompensatoryabilityinresponsetoherbivorythanpopulationsfromlocationswithoutinsectexposurehistory.Whiletherewasalargeinter-populationvariance,thetypeofherbivory(A.hygrophila,C.piperata,orboth)wasnotfoundtoaffectthelevelofcompensation.

DifferencesincompensatoryabilitybetweenplantpopulationswithdifferentgrazinghistorieshavealsobeenreportedinArtemisialudoviciana(DamhoureyehandHartnett2002),Sorghastrumnutans(DamhoureyehandHartnett2002),AgropyronsmithiiRydb(DetlingandPainter1983;PolleyandDetling1988)andBoutelouacurtipendulavar.caespitosa(Smith1998).However,thedifferingintensitiesofcompensatoryresponsebypopulationsofA.philoxeroideswithvaryingherbivoryexposurehistory,andtheclonalnatureoftheplant,suggeststhattheeffectseenheremightbeduetoepigeneticinheritance(McKeyetal.2010;Prentisetal.2008).Indeed,Gaoetal.(2010)reportedthatgenome-wideDNAmethylationalterna-tionsenableA.philoxeroidestoadapttovaryingwateravailabilityrapidly.

Inresponsetolong-termherbivory,aplantmaydisplayevolutionaryorplasticchangesinphysiologyormorphologythatmayincreasecompensatoryability,e.g.formingmorehorizontally-orientedleaves,allo-catingfewerresourcestonewleavesormoreresourcestoroots,orstoringmorereservesbelow-ground(CarmanandBriske1985;MackandThomp-son1982;McIntireandHik2002).Forexample,rametsoftheclonalaquaticplantRanunculus

lingua

Insectexposurehistoryincreasesaninvader’scompensatoryabilityFig.2Impactsof

herbivoryinthegreenhouseexperimentonatotalandbshootmass,andcnumberofrootbudsofplantsexposedorunexposedtoherbivoresinthe eld:meansforindividualpopulations.Valuesarepopulationmeans±1SE(backtransformedforthetotalandshootmass).

Symbolsabovepairsofbarsshowprobability(ttest)thatthetwomeansdidnotdiffer:(nosymbol)[0.05;

*0.01–0.05;**0.001–0.01;***\0.001

655

thathadexperiencedsubstantialherbivoryproducedlargerbutfewerrhizomesandexperiencedlessreductioninmostgrowthparameterswhenexposedtoextensiveherbivory,incomparisonwithrametsthathadexperiencedlessherbivory(Johansson1994).ThegreatercompensatoryabilityofA.philoxeroideswithinsectexposurehistorycomparedtoplantswithoutinsectexposurehistorymayhaveresultedprimarilyfromincreaseinrootstoragemass,whichhasbeenreportedtobehighlycorrelatedwithitscompensatoryability(Wilsonetal.2007;LuandDing2010).

Our ndingthatA.philoxeroidesfrom vepopula-tions(fourwithandonewithoutherbivoryexposurehistory)over-compensatedherbivoryprovidesinsightsintotheplant’sphysiologicalpotentialforcompensa-tion.However,whethertheplantcanovercompensateinresponsetoherbivoryundernatural eldconditionsneedsfurtherclari cation,sinceaplant’scompensa-tionintensityisalsoin uencedbyotherenvironmentalconditions,includingresourceavailability,time,fre-quencyandintensityofdamage,neighbouringplants,anddurationoftherecoveryperiod(MaschinskiandWhitham1989;StraussandAgrawal1999).Schooleretal.(2006,2007)foundthatherbivorysigni cantlysuppressedthegrowthofA.philoxeroideswhentherecoveryperiodwasjust5weeksor

less.

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656X.Lu,J.Ding

Table3Athree-waynestedANOVAfortheeffectsofinsectspecies(Is),population(P),herbivory(H)andtheirinteractionsonplanttotal,rootandshootmass;roottoshootbiomassratio(R/S);totalnumberofbuds;andnumbersofrootandstembudsSourceofvariation

df

TotalbiomassF

InsectspeciesPopulation[Is]HerbivoryIs*HP[Is]*HError

Sourceofvariation

2,55,2411,2412,55,241241df

Totalno.ofbudsF

InsectspeciesPopulation[Is]HerbivoryIs*HP[Is]*HError

2,55,2411,2412,55,241241

0.00217.6906.9000.1042.010

P0.99<0.00010.0090.900.078

No.ofrootbudsF1.0512.9403.7000.5181.150

P0.420.0130.0560.620.33

No.ofstembudsF0.04014.14013.4300.1381.670

P0.96<0.00010.00030.870.14

0.46823.41017.3900.0133.440

P0.65<0.0001<0.00010.990.005

RootmassF0.30214.26032.8200.20071.560

P0.75<0.0001<0.00010.820.17

ShootmassF0.51422.7306.1700.0063.840

P0.63<0.00010.0140.990.002

R/SF0.5028.9707.9800.1312.500

P0.63<0.00010.0050.880.03

Squarebracketsindicatenestingofterms

Statisticallysigni cantvalues(P\0.05)areinbold

Our ndingsmayholdbroadimplicationsforthebiologicalcontrolofinvasiveplants.Introducingandreleasingnaturalenemiesinsomecasesmayfavour,ratherthansuppress,thegrowthoftargetspeciesthroughincreasedcompensatoryresponsetoherbiv-ory—anundesirableoutcome.Theabilityofnativeherbivorestoreduceplantperformanceandincrease

`themortalityofinvasiveplants(MaronandVila

2001),haspromptedthesuggestiontousenativeherbivoresasbiologicalcontrolagents(Croninetal.1999;Mitchelletal.2006).However,thecompensa-torygrowthofA.philoxeroidesinresponsetothenativebeetleinourstudyshowthateventheuseofnativespeciesmaynotalwaysresultincontrol.Thus,toimprovebiocontrolef cacyandavoidpotentialnegativeeffectofbiocontrolagentsonnativeplants,anexplicitunderstandingofthetargetplant’sdefencestrategyiscrucialbeforeapprovalandintroductionofforeignnaturalenemies,aswellastheuseofnativeherbivores.

AcknowledgmentsWethankWenfengGuo,YiWang,XiaJin,HongjunDai,YanSunandKaiWufortheir eldandlabassistance.Themanuscriptwasimprovedbycommentsfrom

¨rer,David¨ller-SchaRichardN.Mack,JohnWilson,HeinzMu

Lodge,AshleyBaldridge,MatthewBarnes,VictoriaNuzzo,

SathyamurthyRaghu,AnjanaDewanji,JianwenZouandthreeanonymousreviewers.ThisworkwasfundedbytheKnowledgeInnovationProgramoftheChineseAcademyofSciencesandtheNationalScienceFoundationofChina(30871650&31100302)whilepreparingthismanuscript.

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