J Appl Entomol 20171ndash9 wileyonlinelibrarycomjournaljen emsp|emsp1copy 2017 Blackwell Verlag GmbH

Received2July2017emsp |emsp Accepted24October2017DOI101111jen12477

O R I G I N A L C O N T R I B U T I O N

Effects of Tomato chlorosis virus on the performance of its key vector Bemisia tabaci in China

J Li1 emsp|emspT B Ding1emsp|emspH Chi2emsp|emspD Chu1

1KeyLaboratoryofIntegratedCropPestManagementofShandongProvinceCollegeofAgronomyandPlantProtectionQingdaoAgriculturalUniversityQingdaoChina2DepartmentofPlantProductionandTechnologiesFacultyofAgriculturalSciencesandTechnologiesNiğdeOumlmerHalisdemirUniversityNiğdeTurkey

CorrespondenceDongChuKeyLabofIntegratedCropPestManagementofShandongProvinceCollegeofAgronomyandPlantProtectionQingdaoAgriculturalUniversityQingdaoChinaEmailchinachudongsinacom

Funding informationNationalNaturalScienceFoundationofChinaGrantAwardNumber31401809High-levelTalentsFundsofQingdaoAgriculturalUniversityGrantAwardNumber631345TaishanMountainScholarConstructiveEngineeringFoundationofShandong

AbstractTomato chlorosis virus(ToCV)whichisanewlyemergedandrapidlyspreadingplantvirusinChinahasseriouslyreducedtomatoproductionandqualityoverthepastsev-eralyearsInthisstudytheeffectofToCVonthedemographyofthewhiteflyBemisia tabacibiotypeQ(HemipteraAleyrodidae)fedoninfectedandhealthytomatoplantswasevaluatedusingtheage-stagetwo-sexlifetableWhenrearedonToCV-infectedtomatoplantsthefecunditylengthofovipositionperiodandfemaleadultlongevityofB tabaci biotypeQ decreased significantly while the pre-adult duration signifi-cantlyincreasedcomparedtocontrolsrearedonhealthytomatoesConsequentlytheintrinsicrateofincrease(r)andfiniteofincrease(λ)ofB tabacibiotypeQonToCV-infectedtomatoplantssignificantlydecreasedcomparedtothoseonhealthytoma-toesPopulationprojectionpredictedthatapopulationofB tabacibiotypeQfedonToCV-infectedtomatoesincreasesslowerthanonhealthyplantsThesefindingsdem-onstratedthatToCVinfectiondecreasedtheperformanceofB tabacibiotypeQontomatoplants

K E Y W O R D S

Bemisia tabacilifetableTomato chlorosis virusvectorperformance

1emsp |emspINTRODUCTION

The sweet potato whitefly Bemisia tabaci (Gennadius) (HemipteraAleyrodidae)whichisconsideredtobeoneofthemosteconomicallyimportantcroppestsworldwidehasinvadedover60countriesduringthepastdecades(DeBarroLiuBoykinampDinsdale2011DinsdaleCook Riginos Buckley ampDeBarro 2010)Bemisia tabaci is a spe-ciescomplexcomposedofat least34morphologically indistinguish-able cryptic species amongwhich B tabaci biotype B (also knownas MEAM1 putative species) and B tabaci biotype Q (also knownasMEDputativespecies)arethetwomostinvasiveanddestructiveforms(BoykinampDeBarro2014DeBarroetal2011)Bemisia tabaci biotypeQwasfirstdetectedinYunnanProvinceChinain2003(Chuetal 2006) andhas sincedisplacedB tabaci biotypeBwhichwasintroducedinthe1990sInrecentyearsB tabacibiotypeQhasbe-comethedominantwhiteflyinthefieldbecomingamajorcroppestinChina(Panetal2011RaoLuoZhangGuoampDevine2011)The

whitefly causes severe crop damage through direct feeding excre-tionofhoneydewandtransmissionofnumerousplantviruses(Jones2003)Twohundredandtwelvevirusspeciesareknowntobetrans-mittedbyB tabaciofwhich906belongtothegenusBegomovirus57inthegenusCrinivirusandtheremaining37distributedamongseveralminorgeneraincludingClosterovirusIpomovirus and Carlavirus (PolstonDeBarroampBoykin2014)

Tomato chlorosis virus (ToCV) (genus Crinivirus familyClosteroviridae) is one of the most devastating tomato pathogensin subtropical regionsworldwideand is responsible for severelyde-creasingtomatoproductionwhereveritbecomesestablished(Navas-Castillo Fiallo-Olive amp Sanchez-Campos 2011 Tzanetakis MartinampWintermantel 2013)ToCV is a phloem-limitedvirus transmittedby severalwhitefly species includingB tabaci Trialeurodes vaporari-orum (Westwood) andT abutilonea (Haldeman) in a semi-persistentnon-circulative manner (Chen etal 2016Wintermantel ampWisler2006)Therelationshipbetweenthevirusandvectorcansignificantly

2emsp |emsp emspensp LI et aL

impact transmission efficiency (Wintermantel Cortea AnchietaGulati-Sakhuja amp Hladky 2008) ToCV outbreaks are frequent inmanypartsof theworld including theAmericas EuropeAfrica anditsadjacentislandstheMiddleEastandAsia(WintermantelampWisler2006Wintermanteletal2008)ToCVwasfirstrecordedinTaiwanin2004(TsaiShihGreenampHanson2004)andoutbreaksofToCVdiseasewithseveresymptomsoccurredinseveralregionsofBeijingTianjinandShandongbetween2012and2016 (Wangetal2016)AfterwardsB tabacibiotypeQwasfoundtobethemajorvectorinToCV-infectedfieldsinChina(DaiLiuZhuLiuampZhao2016)

Increased incidences ofToCV and itswhitefly vectors in green-houseandfieldproductionsystemsacrossnumerousagriculturalcropshave emphasized the need for additional efforts towardsmanagingToCVanditswhiteflyvectorsEffortstoelucidatefactorscontributingtotheemergenceandprevalenceofToCVareimportantforexplainingToCVepidemiologyanddevelopingeffectivemanagementstrategiesforToCVcontrolTherelationshipbetweenpathogenvectorandhostplant is important in understanding the epidemiology of all insect-transmittedplantpathogensConstructionandinterpretinglifetablesisanindispensabletoolingeneratinganoverallassessmentoffitnessofavectoronahostplanttraditionalfemale-basedage-specificlifetables(Birch1948Carey1993Leslie1945Lewis1942)howeverareinherentlyincapableofproperlydescribingapopulationbecausetheyignorethemalecomponentofapopulationandstagestructureinmetamorphosingspeciesAge-stagetwo-sexlifetableconstructionisacomprehensivemethodforsummarizingthesurvivaldevelopmentandreproductivepotentialofapopulation (Chi1988)Becausethismethod can readily portray stage differentiation and includes bothsexesitcanaccuratelydepicttheactuallifehistoryofaninsectspe-ciesThislifetablewhichhasbeenwidelyutilizedinthemeasurementofvariousecologicalaspectsofinterestinrelationtoinsectpestsandtheirnaturalenemiesishelpfultothedevelopmentofintegratedcon-trolstrategies(ChiampSu2006ReddyampChi2015Saskaetal2016YinSunWuampGe2010)

The interactionsbetweenhostplantndashplantvirusndasharthropodvec-torsarecharacterizedbycomplexdirectorindirectinteractionswithmanystudieshavingshownthatsuchcomplexinteractionsmayplayimportantroles intheabundanceanddistributionofarthropodvec-tors and the epidemiology of plant virus diseases (Stout Thaler ampThomma2006)AplantviruscanaffectthearthropodvectordirectlybyinfluencingphysiologicalfunctionsorindirectlybyinfluencinghostplantnutrientexchangesThesechangescanalterthevectorrsquosdevel-opmentlifecyclefertilityandotherlifehistoryparameters(Jiuetal2007LiLiuampLiu2011MatsuuraampHoshino2009RubinsteinampCzosnek1997SidhuMannampButter2009Suetal2015)

ThegoalofthisstudywastounderstandthepotentialeffectsofToCVinfectiononperformanceofB tabacibiotypeQInthisstudythedifferencesofperformanceofB tabacibiotypeQonToCV-infectedandhealthy tomatoplantswere firstevaluatedusing theage-stagetwo-sex life tablewith a simplifiedmethod (Chi 1988 ZhengTaoChiWanampChu2017)Thedifferences in thegrowthpotentialofB tabacibiotypeQonToCV-infectedandhealthytomatoplantswerealsodemonstratedusingpopulationprojections

2emsp |emspMATERIALS AND METHODS

21emsp|emspInsects

ThestockpopulationofB tabacibiotypeQwasobtainedfromalabora-torycolonyestablishedfromJinaShandongChinain2012Thewhite-flieswereculturedoncottonplantsGossypium hirsutumMcvLu-Mian21acommonhostplantofB tabacibiotypeQExperimentalwhiteflyadultsweretransferredtotomatoplantsandrearedforfivegenerationspriortobeingusedTomatoplantsweregrownininsect-proofscreencagesplaced inclimate-controlledcubiclesat27plusmn2degC60plusmn10RHand a photoperiodof 168 (LD) hrAll experimentswere conductedunder identical environmental conditions The purity of theB tabaci biotypeQpopulationwasmaintainedbymonitoring itevery30daysusingtheVspI-basedmtCOIPCR-RFLPmethod(Chuetal2012)

22emsp|emspPlants and ToCV

TomatoplantsSolanum lycopersicumMillCvZhongza9ahostofToCVwereusedinthisstudyVirus-freetomatoplantsweregrowninapottingmix(amixtureofhumussoilvermiculiteorganicfertilizerandperliteina1010101ratiobyvolume)in10-cmdiameterplasticpots inclimate-controlledchambersTheToCVwasobtained fromQingdaoShandongChinain2014andmaintainedontomatoplantsfromtheabovecultureToCV-infectedtomatoplantswereobtainedbymalewhitefly inoculation (malewhiteflieswere transferred andallowedtofeedonToCVtomatoplantsfor48hrandthen30malewhiteflies were transferred onto healthy tomatoes for 5days)Healthytomatoplantswereusedascontrolsexposedtofeedingbynon-viruliferousmalewhiteflies(30non-viruliferousmalewhitefliesweretransferredontohealthytomatoplantsfor5days)Alltomatoplantswereinoculatedatthe4thndash5thtrue-leafstageVirus-infectedandhealthytomatoplantswereusedintheage-stagetwo-sexlifetable experiments approximately 4weeks after inoculation Thevirus infection status of test plantswas visually determinedwhentheplantsshowedtypicalsymptomsandthenverifiedusingreversetranscription-PCR(RT-PCR)asdescribedbyDovasKatisandAvgelis(2002)Allplantswerewateredevery5ndash7daysasnecessary

23emsp|emspDetection of ToCV in tomato plants using the RT- PCR method

Total RNAs from inoculated and control tomato plants were ex-tracted from 100mg of leaf tissue per plant using Trizol reagentfollowing the manufacturerrsquos protocol (Invitrogen Carlsbad CAUSA) The resulting total RNA was resuspended in nuclease-free water and quantified with a NanoPhotometer N50 (ImplenScientific Munich Germany) Reverse transcription was thenperformedon20μgof eachRNA sample The first-strand cDNAwas synthesized using the PrimeScripttrade RT reagent Kit accord-ing to themanufacturerrsquosprotocol (TaKaRaBiotechnologyDalianCoLtdLiaoningChina)Specificprimers (forwardprimerToC-55prime-GGTCAATTATGAGGTCGTGAA-3primeand reverse primer ToC-65prime-CTCTGCCCAGACTTGTAATCA-3prime) were used to detect ToCV

emspensp emsp | emsp3LI et aL

(Dovasetal2002)PCRamplificationswereperformedin20μlofamixturecontaining14μlof cDNA03μlofeachprimer (10μm each)and18μlofPremixTaq(TaKaRaBiotechnologyCorporationCoLtdDalianChina)SimultaneouslyPCRamplificationswiththenegativecontrols(templatewasddH2O)andpositivecontrols(tem-platewasthetomatoplantcDNAcontainingToCV)werealsoper-formedThecyclingconditionswereasfollows4minofactivationat94degCfollowedby35cyclesof30sat94degC30sat55degC30sat72degCandafinalextensionof10minat72degCThePCRproductswereelectrophoresedona12agarosegel ina05timesTBEbufferandwerevisualizedbyGelviewstaining

24emsp|emspPopulation parameters of B tabaci biotype Q on ToCV- infected and healthy tomato plants

To determine differences in the population parameters ofB tabaci biotypeQonToCV-infectedandhealthytomatoplantsweanalysedthe population parameters using the age-stage two-sex life tablemethod(Chi1988ChiampLiu1985)Forthelifetablestudytherear-ingcontainers(FigS1)weremadeofplasticpotsAsmallpot(7cmtopdiameter45cmbottomdiameterand75cmheight)whichwasusedasthebottomcontainerwascoveredwithplasticwraptoisolatethewhitefliesfromgroundwaterAninvertedplasticpot(75cmtopdiameter5cmbottomdiameterand11cmheight)wasusedasthecoverThetopoftheplasticpotcoverwascutoutandcoveredwithfinemeshclothforventilationTomatoseedlingsatthe7thndash9thleafstagewereusedinthisstudyAsingletrueleaf(thirdtoseventhleaffrom thebottom)wasdetached from the tomato seedling and thestemofthetrueleafimmersedin1-naphthylaceticacid(50ppm)for10minrinsedwithwaterandthenmaintainedinaseparatecontainerwithnutrientsolution(LvSangLiampLi2010)

Life table experiments were conducted in climate-controlledchambersat27plusmn2degC60plusmn10relativehumidityandaphotoperiodof168(LD)hrApproximately10pairsofwhiteflyadults(randomlyselected from the culturepopulationmaintainedon tomatoplants)were transferred into rearingcontainerscontainingasingle tomatoseedling The same process was repeated on healthy tomato andToCV-infected tomato plants Each treatment contained four repli-catesAfter24hralloftheadultswereremovedandthenumbersofeggscountedunderastereomicroscope(NikonSMZ745T)Therewere155and125eggsusedforthelifetablestudiesonhealthyandToCV-infectedtomatoplantsrespectivelyTheseedlingsintherear-ingcontainerswerecheckeddaily fornewlyemergedadultsbegin-ningatthe15thday(correspondingtothedaypriortoeclosion)Dateforthepre-adultdurationandpre-adultsurvivalwasrecordedforallindividuals Newly emerged female andmale adults resulting fromthetreatmentwerepairedandtransferredtoanewrearingcontainerwithcontainingatomatoleafandallowedtomateandovipositTheadultwhitefly individualswerecheckeddailyforsurvivalTorecordeggproductioneachpairofthewhiteflieswastransferredintoanewrearingcontainerwithonetomatoleafevery5days(correspondingtothetimeperiodpriortonymphemergence)Thedailyfecunditywascalculatedasthemeannumberofeggslaidwithineach5-dayperiod

25emsp|emspStatistical analysis

Therawlifehistorydataofallthewhiteflyindividualswereanalysedbasedontheage-stagetwo-sexlifetable(Chi1988ChiampLiu1985)using the computer program TWOSEX-MSChart (Chi 2017) Theprogram isavailable fornocostathttp140120197173EcologydownloadTWOSEX-MSChartrarThepopulationparametersincludedtheage-stagespecificsurvivalrate(sxjtheprobabilitythatanewbornwillsurvivetoagexandstage j)theage-specificsurvivalrate(lxtheprobabilityofanewlylaideggsurvivingtoagex)theage-stage-specificfecundity(fxjthemeannumberofoffspringproducedbyafemaleatagex)theage-specificfecundity(mxthemeanfecundityofindividualsatagex)theage-stagelifeexpectancy(exjthelengthoftimethatanindividualofagexandstagejisexpectedtolive)andthereproductivevalue (vxjthecontributionofanindividualtothefuturepopulation)

Intheage-stagetwo-sexlifetable(ChiampLiu1985)mx and lx are calculatedas

wherekisthenumberofstagesThenetreproductiverate(R0)iscal-culatedas

The intrinsic rate of increase (r) is determined using the EulerndashLotkaequation

with age is indexed from0 (Goodman 1982)The finite rate of in-crease(λ)iscalculatedasλ = erThemeangenerationtimeTisdefinedas the lengthof timethatapopulationneedsto increaseR0 foldofitssize(ieerT = R0 or λT = R0)atastableage-stagedistributionandiscalculatedas

The life expectancyexj is calculated as describedbyChi andSu(2006)as

wheresprimeiyistheprobabilitythatanindividualofagexandstagej will survivetoageiandstageyandiscalculatedbyassumingsprimexj=1(ChiampSu2006)Thereproductivevalue(vxj)iscalculatedaccordingtoTuanLeeandChi(2014ab)as

(1)mx=

ksum

j=1

sxjfxj

ksum

j=1

sxj

(2)lx=

ksum

j=1

sxj

(3)R0=

infinsum

x=0

lxmx

(4)

infinsum

x=0

eminusr(x+1)lxmx=1

(5)T=lnR0

r

(6)exj=

infinsum

i=x

ksum

y=j

siy

emspensp emsp | emsp3LI et aL

(Dovasetal2002)PCRamplificationswereperformedin20μlofamixturecontaining14μlof cDNA03μlofeachprimer (10μm each)and18μlofPremixTaq(TaKaRaBiotechnologyCorporationCoLtdDalianChina)SimultaneouslyPCRamplificationswiththenegativecontrols(templatewasddH2O)andpositivecontrols(tem-platewasthetomatoplantcDNAcontainingToCV)werealsoper-formedThecyclingconditionswereasfollows4minofactivationat94degCfollowedby35cyclesof30sat94degC30sat55degC30sat72degCandafinalextensionof10minat72degCThePCRproductswereelectrophoresedona12agarosegel ina05timesTBEbufferandwerevisualizedbyGelviewstaining

24emsp|emspPopulation parameters of B tabaci biotype Q on ToCV- infected and healthy tomato plants

To determine differences in the population parameters ofB tabaci biotypeQonToCV-infectedandhealthytomatoplantsweanalysedthe population parameters using the age-stage two-sex life tablemethod(Chi1988ChiampLiu1985)Forthelifetablestudytherear-ingcontainers(FigS1)weremadeofplasticpotsAsmallpot(7cmtopdiameter45cmbottomdiameterand75cmheight)whichwasusedasthebottomcontainerwascoveredwithplasticwraptoisolatethewhitefliesfromgroundwaterAninvertedplasticpot(75cmtopdiameter5cmbottomdiameterand11cmheight)wasusedasthecoverThetopoftheplasticpotcoverwascutoutandcoveredwithfinemeshclothforventilationTomatoseedlingsatthe7thndash9thleafstagewereusedinthisstudyAsingletrueleaf(thirdtoseventhleaffrom thebottom)wasdetached from the tomato seedling and thestemofthetrueleafimmersedin1-naphthylaceticacid(50ppm)for10minrinsedwithwaterandthenmaintainedinaseparatecontainerwithnutrientsolution(LvSangLiampLi2010)

Life table experiments were conducted in climate-controlledchambersat27plusmn2degC60plusmn10relativehumidityandaphotoperiodof168(LD)hrApproximately10pairsofwhiteflyadults(randomlyselected from the culturepopulationmaintainedon tomatoplants)were transferred into rearingcontainerscontainingasingle tomatoseedling The same process was repeated on healthy tomato andToCV-infected tomato plants Each treatment contained four repli-catesAfter24hralloftheadultswereremovedandthenumbersofeggscountedunderastereomicroscope(NikonSMZ745T)Therewere155and125eggsusedforthelifetablestudiesonhealthyandToCV-infectedtomatoplantsrespectivelyTheseedlingsintherear-ingcontainerswerecheckeddaily fornewlyemergedadultsbegin-ningatthe15thday(correspondingtothedaypriortoeclosion)Dateforthepre-adultdurationandpre-adultsurvivalwasrecordedforallindividuals Newly emerged female andmale adults resulting fromthetreatmentwerepairedandtransferredtoanewrearingcontainerwithcontainingatomatoleafandallowedtomateandovipositTheadultwhitefly individualswerecheckeddailyforsurvivalTorecordeggproductioneachpairofthewhiteflieswastransferredintoanewrearingcontainerwithonetomatoleafevery5days(correspondingtothetimeperiodpriortonymphemergence)Thedailyfecunditywascalculatedasthemeannumberofeggslaidwithineach5-dayperiod

25emsp|emspStatistical analysis

Therawlifehistorydataofallthewhiteflyindividualswereanalysedbasedontheage-stagetwo-sexlifetable(Chi1988ChiampLiu1985)using the computer program TWOSEX-MSChart (Chi 2017) Theprogram isavailable fornocostathttp140120197173EcologydownloadTWOSEX-MSChartrarThepopulationparametersincludedtheage-stagespecificsurvivalrate(sxjtheprobabilitythatanewbornwillsurvivetoagexandstage j)theage-specificsurvivalrate(lxtheprobabilityofanewlylaideggsurvivingtoagex)theage-stage-specificfecundity(fxjthemeannumberofoffspringproducedbyafemaleatagex)theage-specificfecundity(mxthemeanfecundityofindividualsatagex)theage-stagelifeexpectancy(exjthelengthoftimethatanindividualofagexandstagejisexpectedtolive)andthereproductivevalue (vxjthecontributionofanindividualtothefuturepopulation)

Intheage-stagetwo-sexlifetable(ChiampLiu1985)mx and lx are calculatedas

wherekisthenumberofstagesThenetreproductiverate(R0)iscal-culatedas

The intrinsic rate of increase (r) is determined using the EulerndashLotkaequation

with age is indexed from0 (Goodman 1982)The finite rate of in-crease(λ)iscalculatedasλ = erThemeangenerationtimeTisdefinedas the lengthof timethatapopulationneedsto increaseR0 foldofitssize(ieerT = R0 or λT = R0)atastableage-stagedistributionandiscalculatedas

The life expectancyexj is calculated as describedbyChi andSu(2006)as

wheresprimeiyistheprobabilitythatanindividualofagexandstagej will survivetoageiandstageyandiscalculatedbyassumingsprimexj=1(ChiampSu2006)Thereproductivevalue(vxj)iscalculatedaccordingtoTuanLeeandChi(2014ab)as

(1)mx=

ksum

j=1

sxjfxj

ksum

j=1

sxj

(2)lx=

ksum

j=1

sxj

(3)R0=

infinsum

x=0

lxmx

(4)

infinsum

x=0

eminusr(x+1)lxmx=1

(5)T=lnR0

r

(6)exj=

infinsum

i=x

ksum

y=j

siy

4emsp |emsp emspensp LI et aL

ThestandarderrorsofalllifetableparametersincludingrλR0Tadultlongevityandfecunditywereestimatedusingthebootstrappro-cedurewith100000resamplingApairedbootstraptestwasusedtodetectthedifferencebetweentreatmentsbasedontheconfidencein-tervalofdifferences(Polat-AkkoumlpruumlAtlihanOkutampChi2015EfronampTibshirani 1993HuangampChi 2012) SigmaPlotv120 softwarewasusedtopreparethegraphs

26emsp|emspPopulation projection

Weprojectedthepopulationgrowthtoillustratethepredictedpopula-tionsizeandage-stagestructureofaB tabacipopulationbyincorporatingdevelopmentalratesurvivalrateandfecunditydata(Chi1990ChiampLiu1985) using the TIMING-MSChart program (http140120197173ecologyDownloadTIMING-MSChartrar)(Chi2016)

3emsp |emspRESULTS

31emsp|emspDetection of ToCV in tomato plants using RT- PCR method

TheprimersToc-5andToc-6amplifiedafragmentofexpectedsizefrom extracts from individual tomato plants that had been inocu-latedwithToCV(Figure1a)Noproductwasobtainedfromthenon-inoculatedtomatoplants(Figure1b)

32emsp|emspPopulation parameters of whiteflies on ToCV- infected and healthy tomato plants

Whitefly pre-adults developed slower on ToCV-infected tomatoplants than on healthy tomato plants The pre-adult duration266plusmn037days when reared on ToCV-infected tomato plantswas significantly longer than that observed on healthy plants(2365plusmn031days p lt 0001) (Table1) However the longevityof female adults was significantly shorter when reared on ToCV-infected tomato plants (206plusmn094days) than on healthy plants(2384plusmn081days) (p = 0098) (Table1) Themean fecundity of fe-maleswas9210plusmn655eggsonToCV-infectedplants a significant

decrease when compared to the mean fecundity of 13037plusmn434eggs on healthy tomato plants (p lt 0001) (Table1) Therewere nosignificantdifferencesinthepre-adultsurvivalrateandmalelongev-itybetweenToCV-infectedandhealthytomatoplants(p = 3903andp = 7381respectively)(Table1)

TherelativelyslowdevelopmentofB tabacibiotypeQonToCV-infected plants could also be observed in the age-stage survivalrate(sxj)whereadultsofbothsexesbegantoemergeafter21days(Figure2b)onToCV-infectedtomatoplantsversus19daysonunin-fectedplants(Figure2a)Thefemaleage-stagespecificfecundity(fxj)andage-specificfecundity(mx)onToCV-infectedtomatoplantsbeganonthe20thday(Figure3b)only1daylaterthanonhealthyplants(atday19)(Figure3a)Allmxlxmx and fxjvaluesonToCV-infectedtomatoplantswerelowerthanthoseonhealthytomato(Figure3)

The intrinsicrateof increase (r) finiterate (λ)andnetreproduc-tiverate(R0)ofwhitefliesrearedonToCV-infectedtomatoplantswere010plusmn0005dminus1 111plusmn0005dminus1 and 3463plusmn468 eggs respec-tivelyandallofwhichweresignificantlylowervalues(p lt 0001)thanthose on healthy tomato plants (013plusmn0003dminus1 114plusmn0004dminus1 and6729plusmn570 eggs respectively) (Table2)Themean generationtime(T)onToCV-infectedtomatoplants(3441plusmn072days)waslon-gerthanthatonhealthytomatoplants(3155plusmn042days)(p = 0007)(Table2)

Themeanlongevityofthewhitefliesthatisthelifeexpectancyatagezero(e01)was417daysonToCV-infectedtomatoplantswhichwassimilartothatonhealthyplants(413days)(Figure4)Atagezerothereproductivevalues(v01)wereequivalenttothefiniteratesonbothplantsthatis11085dminus1onToCV-infectedtomatoand11427dminus1 on healthy tomato (Figure5)The vxj values jumped to 452845d

minus1 on day19when female adults emergedonhealthy tomatoplants and475343dminus1when they emerged later (on day 20)when reared onToCV-infectedplants(Figure5)

33emsp|emspPopulation projection of the whitefly on ToCV- infected and healthy tomato plants

Thepopulationsizesofthedifferentstagessimulatedfromaninitialpopulationof10eggsusingtheTIMING-MSChartprogramareshowninFigure6ThewhiteflypopulationincreasedmuchsloweronToCV-infectedtomatoplantsthanonhealthyplants(Figure6)After60daysonToCV-infectedtomatoplantstherewere1318individualsinvari-ouspre-adultstages49femaleand57maleadultswhileonhealthy

(7)vxj=er(x+1)

sxj

infinsum

i=x

eminusr(i+1)ksum

y=j

siyfiy

F IGURE 1emspDetectionofToCVintomatoplantsbyRT-PCRandagarosegelelectrophoresiswithGelviewstainingEachlaneisaPCRamplificationfromtheRNAextractionofoneleafofeachtomatoplant(a)SampleswerefromtomatoplantsinoculatedwithToCVafter3weeks(lanes3-24)(b)Sampleswerefromhealthytomatoplants(lanes3-24)laneM2000bpmarkerlane1apositivesampleofToCV-infectedtomatoplantlane2anon-inoculatedcontroltomatoplant

(a)

(b)

emspensp emsp | emsp5LI et aL

tomatoplants therewere9752 individuals in thepre-adult stages171femaleand116maleadults(Figure6)

4emsp |emspDISCUSSION

InthisstudytheimpactofToCVinfectiononpopulationparametersof B tabaci biotype Q was examined using the age-stage two-sexlife table Thismethodwas chosen because contrary to traditional

female-based life tables it is capable of precisely describing thepopulationparametersstagedifferentiationandvariationamongin-dividualsby takingbothsexes intoconsideration (Chi1988ChiampLiu1985)Our results showed that the fecundityand femaleadultlongevity ofB tabaci biotypeQwere significantly decreasedwhilethepre-adultduration(fromeggtoadult)wassignificantlyextendedwhen reared on ToCV-infected tomato plants comparedwith theircounterpartsrearedonhealthytomatoplants(Table1)MannSidhuButterSohiandSekhon(2008)andSidhuetal(2009)reportedsimilar

Basic statistic

Host plant

n Healthy tomato n ToCV- infected tomato p

Pre-adultduration(days)

128 2365plusmn031 98 2666plusmn037 0001

Pre-adultsurvivalrate()

155 8258plusmn304 125 7840plusmn37 3903

Femalelongevity(days)

80 2384plusmn081 47 2060plusmn094 0098

Malelongevity(days)

48 2051plusmn137 51 1994plusmn102 7381

Ovipositiondays(days)

80 2206plusmn072 47 1887plusmn091 0062

Fecundity(eggsperfemale)

80 13037plusmn434 47 9210plusmn655 0000

TABLE 1emspMeansandstandarderrorsofpre-adultdevelopmentaltime(days)pre-adultsurvivalrate()adultlongevity(days)ovipositiondays(days)andfecundity(eggs)ofB tabaciQonhealthyandToCV-infectedtomatoStandarderrorswereestimatedusing100000bootstrapresamplingThedifferencesbetweentwotreatmentswereevaluatedusingpairedbootstraptest

F IGURE 2emspAge-stage-specificsurvivalrate(sxj)oftheB tabaci biotypeQonhealthyandToCV-infectedtomatoplant

F IGURE 3emspAge-specificsurvivalrate(lx)femaleage-specificfecundity(fxj)age-specificfecundityofthetotalpopulation(mx)andage-specificmaternity(lxmx)oftheB tabacibiotypeQonhealthyandToCV-infectedtomatoplant

6emsp |emsp emspensp LI et aL

resultsforB tabaciovipositingfewereggsandhavingashorterlon-gevityonplantinfectedwithCotton leaf curl virus(CLCuV)RubinsteinandCzosnek (1997) also demonstrated thatTomato yellow leaf curl virus (TYLCV) had adverse effects onB tabaci causing reduced fe-cundityandlongevityJiuetal(2007)alsoreportedsimilareffectsinB tabacicausedbyTomato yellow leaf curl China virus(TYLCCV)AlloftheabovestudiesdemonstratednegativeeffectsthatviruseshadontheirvectorsHoweverPanetal(2013)demonstratedtheopposite

occurredwhenTYLCV-infectedwhitefliesdevelopedahigherfecun-dityandlonger longevitySeveralpreviousreportshaveshownthatcirculativeviruses could increase thequalityof thehostplants andhaveapositiveimpactonthevectorfitnessthroughdownregulationofdefencepathwaysreducedcallosedepositionalteredaminoacidcontentofthesapetc(Casteeletal2015Suetal2015XuHeZhengYangamp Lu 2014) In contrast the effect of non-circulativevirusesonvectorgrowthismuchlessclearBasedontheassumptionthatvirusescanaffecttheinteractionbetweenhostplantsandtheirvectorsplantsinfectedbynon-circulativevirusesshouldrapidlydetervectorsforcingmigrationontoneighbouringhealthyplants(BlancampMichalakis2016)ThusadecreaseinthefitnessofthewhiteflyonitsToCV-infectedtomatoplantmaybeassociatedwithadecreaseinthequalityofthehostplant

Comparisonsofthepopulationparametersespeciallytherλ and R0 valueshavebeengenerallyusedtodetectdifferencesbetweenpopu-lationsortreatmentsBecausetraditionalfemaleage-specificlifetablesignorestagedifferentiationandthemalepopulationtheirapplicationtospecieswithbisexualpopulationswilloftenresultinerrors(HuangampChi2011)InthisstudyweanalyzedandcomparedlifetablesofB ta-bacibiotypeQrearedonhealthytomatoplantsandonToCV-infectedtomatoplantsusingtheage-stagetwo-sexlifetableTherλ and R0 valuesshowedthatB tabacibiotypeQsurvivedbetteronhealthyto-matoplantsthanonToCV-infectedtomatoplants(Table2)Population

TABLE 2emspMeansandstandarderrorsoftheintrinsicrateofincrease(r)finiterate(λ)netreproductiverate(R0)andmeangenerationtime(T)ofB tabaciQonhealthyandToCV-infectedtomatoStandarderrorswereestimatedusing100000bootstrapresamplingApairedbootstraptestwasusedtodetectdifferencesbetweentreatments

Parameters

Host plant

Healthy tomato ToCV- infected tomato p

r (dminus1) 01334plusmn00033 01030plusmn00046 0001

λ (dminus1) 11427plusmn00037 11085plusmn00051 0001

R0(offspringindividual)

6729plusmn570 3463plusmn468 0001

T(days) 3155plusmn042 3441plusmn072 0007

F IGURE 4emspAge-stage-specificlifeexpectancy(exj)oftheB tabaci biotypeQonhealthyandToCV-infectedtomatoplants

F IGURE 5emspReproductivevalue(vxj)oftheB tabacibiotypeQonhealthyandToCV-infectedtomatoplants

emspensp emsp | emsp7LI et aL

projections based on the age-stage two-sex life table can predictchangesinpopulationsizeandstagestructurethroughtimeThesecanbeuseful inprovidingvaluable informationon the trendsandemer-gencetimingofnotonlythepre-adultstagesbutthefemaleandmaleadultemergencesaswell(Chi1990)OurprojectionsdemonstratedthediminishedgrowthofaB tabacipopulationonToCV-infectedtomatoplantscomparedtoapopulationgrowingonhealthyplants(Figure6)EarlierstudiesbyDonaldsonandGratton(2007)alsoreportedthatsoy-beanplants infectedwiththepotyvirusSoybean mosaic virus (SMVanon-persistentvirus)reducedthepopulationgrowthofitsvectoraphidAphis glycinesThisinformationisalsousefulforimplementingandtim-ingpestandplantviruscontrolschedules

Thepresent studydemonstrates thatToCV infections in tomatoplants have detrimental effects onB tabaci biotypeQThis is con-sistentwith theresultspublishedbyFereresetal (2016) thatToCVinfectionpromotedasharpincreaseintheemissionofsometomatoterpenes and non-viruliferouswhiteflies avoided the volatiles fromtheToCV-infectedplantsAllofthesefindingssuggestthatToCVin-fectionisdetrimentaltofurtherspreadoftheToCVwhichwouldseemcontradictorytotheobservedepidemicsoftheToCVinthefieldForexample inafieldsurveyconductedin2014weobservedB tabaci biotype Q outbreaks on ToCV-infected tomato plants in QingdaoShandongProvinceofChina(JLiunpublisheddata)Daietal(2016)

also foundB tabaci biotypeQ outbreaks onToCV-infected tomatoplantsinShouguangShandongChinaPossibleexplanationsforthisareasfollowsToCVinfectionintomatoplantscanlowertheperfor-manceofB tabacibiotypeQbut itmaynotaffecttheefficiencyofvirus acquisition virus retention andor virus transmission Similarresults have been observed in aphids Pentildeaflor Mauck Alves DeMoraesandMescher(2016)foundthatalthoughSMVisdetrimentalto the performance ofA glycines it did not affect the transmissionofSMVInadditionsomestudiesreportedthatthevisualstimulioftheToCV-infectedtomatoplantmaypositivelyaffectwhiteflyprefer-enceirrespectiveoftheirinfectiousstatustheyalwayspreferredtolandonToCV-infectedratherthanonmock-inoculatedleaves(Fereresetal2016)whichwouldbebeneficialtothespreadofToCVBecauseof the complicate interactions amongvirus insectvectors andhostplants the mechanism underlying the epidemics of ToCV in Chinashouldbefurtherexplored

ACKNOWLEDGEMENTS

This work was supported by grants from the National NaturalScience Foundation of China (31401809) the High-level TalentsFunds of Qingdao Agricultural University (631345) and theTaishanMountainScholarConstructiveEngineeringFoundationofShandong

AUTHOR CONTRIBUTION

DC and JL contributed to experimental design and managementJL performed the experiments analyzed the data and drafted themanuscript TBD helped with the experiments HC and DC editedandrevisedthemanuscriptAllauthorsreadandapprovedthefinalmanuscript

ORCID

J Li httporcidorg0000-0002-9013-6862

REFERENCES

Birch L C (1948) The intrinsic rate of natural increase of an in-sect population Journal of Animal Ecology 17 15ndash26 httpsdoiorg1023071605

Blanc S amp Michalakis Y (2016) Manipulation of hosts and vec-tors by plant viruses and impact of the environment Current Opinion in Insect Science 16 36ndash43 httpsdoiorg101016jcois201605007

BoykinLMampDeBarroPJ(2014)Apracticalguidetoidentifyingmem-bersoftheBemisia tabacispeciescomplexAndothermorphologicallyidenticalspeciesFrontiers in Ecology and Evolution245

CareyJR(1993)Applied demography for biologists with special emphasis on insectsNewYorkNYOxfordUniversityPress

CasteelCLDeAlwisMBakADongHWhithamSAampJanderG (2015) Disruption of ethylene responses by Turnip mosaic virus mediatessuppressionofplantdefenseagainstthegreenpeachaphidvector Plant Physiology 169 209ndash218 httpsdoiorg101104pp1500332

F IGURE 6emspPopulationprojectionoftheB tabacibiotypeQonhealthyandToCV-infectedtomatoplantsAninitialpopulationof10eggswasusedineachprojection

6emsp |emsp emspensp LI et aL

resultsforB tabaciovipositingfewereggsandhavingashorterlon-gevityonplantinfectedwithCotton leaf curl virus(CLCuV)RubinsteinandCzosnek (1997) also demonstrated thatTomato yellow leaf curl virus (TYLCV) had adverse effects onB tabaci causing reduced fe-cundityandlongevityJiuetal(2007)alsoreportedsimilareffectsinB tabacicausedbyTomato yellow leaf curl China virus(TYLCCV)AlloftheabovestudiesdemonstratednegativeeffectsthatviruseshadontheirvectorsHoweverPanetal(2013)demonstratedtheopposite

occurredwhenTYLCV-infectedwhitefliesdevelopedahigherfecun-dityandlonger longevitySeveralpreviousreportshaveshownthatcirculativeviruses could increase thequalityof thehostplants andhaveapositiveimpactonthevectorfitnessthroughdownregulationofdefencepathwaysreducedcallosedepositionalteredaminoacidcontentofthesapetc(Casteeletal2015Suetal2015XuHeZhengYangamp Lu 2014) In contrast the effect of non-circulativevirusesonvectorgrowthismuchlessclearBasedontheassumptionthatvirusescanaffecttheinteractionbetweenhostplantsandtheirvectorsplantsinfectedbynon-circulativevirusesshouldrapidlydetervectorsforcingmigrationontoneighbouringhealthyplants(BlancampMichalakis2016)ThusadecreaseinthefitnessofthewhiteflyonitsToCV-infectedtomatoplantmaybeassociatedwithadecreaseinthequalityofthehostplant

Comparisonsofthepopulationparametersespeciallytherλ and R0 valueshavebeengenerallyusedtodetectdifferencesbetweenpopu-lationsortreatmentsBecausetraditionalfemaleage-specificlifetablesignorestagedifferentiationandthemalepopulationtheirapplicationtospecieswithbisexualpopulationswilloftenresultinerrors(HuangampChi2011)InthisstudyweanalyzedandcomparedlifetablesofB ta-bacibiotypeQrearedonhealthytomatoplantsandonToCV-infectedtomatoplantsusingtheage-stagetwo-sexlifetableTherλ and R0 valuesshowedthatB tabacibiotypeQsurvivedbetteronhealthyto-matoplantsthanonToCV-infectedtomatoplants(Table2)Population

TABLE 2emspMeansandstandarderrorsoftheintrinsicrateofincrease(r)finiterate(λ)netreproductiverate(R0)andmeangenerationtime(T)ofB tabaciQonhealthyandToCV-infectedtomatoStandarderrorswereestimatedusing100000bootstrapresamplingApairedbootstraptestwasusedtodetectdifferencesbetweentreatments

Parameters

Host plant

Healthy tomato ToCV- infected tomato p

r (dminus1) 01334plusmn00033 01030plusmn00046 0001

λ (dminus1) 11427plusmn00037 11085plusmn00051 0001

R0(offspringindividual)

6729plusmn570 3463plusmn468 0001

T(days) 3155plusmn042 3441plusmn072 0007

F IGURE 4emspAge-stage-specificlifeexpectancy(exj)oftheB tabaci biotypeQonhealthyandToCV-infectedtomatoplants

F IGURE 5emspReproductivevalue(vxj)oftheB tabacibiotypeQonhealthyandToCV-infectedtomatoplants

emspensp emsp | emsp7LI et aL

projections based on the age-stage two-sex life table can predictchangesinpopulationsizeandstagestructurethroughtimeThesecanbeuseful inprovidingvaluable informationon the trendsandemer-gencetimingofnotonlythepre-adultstagesbutthefemaleandmaleadultemergencesaswell(Chi1990)OurprojectionsdemonstratedthediminishedgrowthofaB tabacipopulationonToCV-infectedtomatoplantscomparedtoapopulationgrowingonhealthyplants(Figure6)EarlierstudiesbyDonaldsonandGratton(2007)alsoreportedthatsoy-beanplants infectedwiththepotyvirusSoybean mosaic virus (SMVanon-persistentvirus)reducedthepopulationgrowthofitsvectoraphidAphis glycinesThisinformationisalsousefulforimplementingandtim-ingpestandplantviruscontrolschedules

Thepresent studydemonstrates thatToCV infections in tomatoplants have detrimental effects onB tabaci biotypeQThis is con-sistentwith theresultspublishedbyFereresetal (2016) thatToCVinfectionpromotedasharpincreaseintheemissionofsometomatoterpenes and non-viruliferouswhiteflies avoided the volatiles fromtheToCV-infectedplantsAllofthesefindingssuggestthatToCVin-fectionisdetrimentaltofurtherspreadoftheToCVwhichwouldseemcontradictorytotheobservedepidemicsoftheToCVinthefieldForexample inafieldsurveyconductedin2014weobservedB tabaci biotype Q outbreaks on ToCV-infected tomato plants in QingdaoShandongProvinceofChina(JLiunpublisheddata)Daietal(2016)

also foundB tabaci biotypeQ outbreaks onToCV-infected tomatoplantsinShouguangShandongChinaPossibleexplanationsforthisareasfollowsToCVinfectionintomatoplantscanlowertheperfor-manceofB tabacibiotypeQbut itmaynotaffecttheefficiencyofvirus acquisition virus retention andor virus transmission Similarresults have been observed in aphids Pentildeaflor Mauck Alves DeMoraesandMescher(2016)foundthatalthoughSMVisdetrimentalto the performance ofA glycines it did not affect the transmissionofSMVInadditionsomestudiesreportedthatthevisualstimulioftheToCV-infectedtomatoplantmaypositivelyaffectwhiteflyprefer-enceirrespectiveoftheirinfectiousstatustheyalwayspreferredtolandonToCV-infectedratherthanonmock-inoculatedleaves(Fereresetal2016)whichwouldbebeneficialtothespreadofToCVBecauseof the complicate interactions amongvirus insectvectors andhostplants the mechanism underlying the epidemics of ToCV in Chinashouldbefurtherexplored

ACKNOWLEDGEMENTS

This work was supported by grants from the National NaturalScience Foundation of China (31401809) the High-level TalentsFunds of Qingdao Agricultural University (631345) and theTaishanMountainScholarConstructiveEngineeringFoundationofShandong

AUTHOR CONTRIBUTION

DC and JL contributed to experimental design and managementJL performed the experiments analyzed the data and drafted themanuscript TBD helped with the experiments HC and DC editedandrevisedthemanuscriptAllauthorsreadandapprovedthefinalmanuscript

ORCID

J Li httporcidorg0000-0002-9013-6862

REFERENCES

Birch L C (1948) The intrinsic rate of natural increase of an in-sect population Journal of Animal Ecology 17 15ndash26 httpsdoiorg1023071605

Blanc S amp Michalakis Y (2016) Manipulation of hosts and vec-tors by plant viruses and impact of the environment Current Opinion in Insect Science 16 36ndash43 httpsdoiorg101016jcois201605007

BoykinLMampDeBarroPJ(2014)Apracticalguidetoidentifyingmem-bersoftheBemisia tabacispeciescomplexAndothermorphologicallyidenticalspeciesFrontiers in Ecology and Evolution245

CareyJR(1993)Applied demography for biologists with special emphasis on insectsNewYorkNYOxfordUniversityPress

CasteelCLDeAlwisMBakADongHWhithamSAampJanderG (2015) Disruption of ethylene responses by Turnip mosaic virus mediatessuppressionofplantdefenseagainstthegreenpeachaphidvector Plant Physiology 169 209ndash218 httpsdoiorg101104pp1500332

F IGURE 6emspPopulationprojectionoftheB tabacibiotypeQonhealthyandToCV-infectedtomatoplantsAninitialpopulationof10eggswasusedineachprojection

emspensp emsp | emsp7LI et aL

projections based on the age-stage two-sex life table can predictchangesinpopulationsizeandstagestructurethroughtimeThesecanbeuseful inprovidingvaluable informationon the trendsandemer-gencetimingofnotonlythepre-adultstagesbutthefemaleandmaleadultemergencesaswell(Chi1990)OurprojectionsdemonstratedthediminishedgrowthofaB tabacipopulationonToCV-infectedtomatoplantscomparedtoapopulationgrowingonhealthyplants(Figure6)EarlierstudiesbyDonaldsonandGratton(2007)alsoreportedthatsoy-beanplants infectedwiththepotyvirusSoybean mosaic virus (SMVanon-persistentvirus)reducedthepopulationgrowthofitsvectoraphidAphis glycinesThisinformationisalsousefulforimplementingandtim-ingpestandplantviruscontrolschedules

Thepresent studydemonstrates thatToCV infections in tomatoplants have detrimental effects onB tabaci biotypeQThis is con-sistentwith theresultspublishedbyFereresetal (2016) thatToCVinfectionpromotedasharpincreaseintheemissionofsometomatoterpenes and non-viruliferouswhiteflies avoided the volatiles fromtheToCV-infectedplantsAllofthesefindingssuggestthatToCVin-fectionisdetrimentaltofurtherspreadoftheToCVwhichwouldseemcontradictorytotheobservedepidemicsoftheToCVinthefieldForexample inafieldsurveyconductedin2014weobservedB tabaci biotype Q outbreaks on ToCV-infected tomato plants in QingdaoShandongProvinceofChina(JLiunpublisheddata)Daietal(2016)

also foundB tabaci biotypeQ outbreaks onToCV-infected tomatoplantsinShouguangShandongChinaPossibleexplanationsforthisareasfollowsToCVinfectionintomatoplantscanlowertheperfor-manceofB tabacibiotypeQbut itmaynotaffecttheefficiencyofvirus acquisition virus retention andor virus transmission Similarresults have been observed in aphids Pentildeaflor Mauck Alves DeMoraesandMescher(2016)foundthatalthoughSMVisdetrimentalto the performance ofA glycines it did not affect the transmissionofSMVInadditionsomestudiesreportedthatthevisualstimulioftheToCV-infectedtomatoplantmaypositivelyaffectwhiteflyprefer-enceirrespectiveoftheirinfectiousstatustheyalwayspreferredtolandonToCV-infectedratherthanonmock-inoculatedleaves(Fereresetal2016)whichwouldbebeneficialtothespreadofToCVBecauseof the complicate interactions amongvirus insectvectors andhostplants the mechanism underlying the epidemics of ToCV in Chinashouldbefurtherexplored

ACKNOWLEDGEMENTS

This work was supported by grants from the National NaturalScience Foundation of China (31401809) the High-level TalentsFunds of Qingdao Agricultural University (631345) and theTaishanMountainScholarConstructiveEngineeringFoundationofShandong

AUTHOR CONTRIBUTION

DC and JL contributed to experimental design and managementJL performed the experiments analyzed the data and drafted themanuscript TBD helped with the experiments HC and DC editedandrevisedthemanuscriptAllauthorsreadandapprovedthefinalmanuscript

ORCID

J Li httporcidorg0000-0002-9013-6862

REFERENCES

Birch L C (1948) The intrinsic rate of natural increase of an in-sect population Journal of Animal Ecology 17 15ndash26 httpsdoiorg1023071605

Blanc S amp Michalakis Y (2016) Manipulation of hosts and vec-tors by plant viruses and impact of the environment Current Opinion in Insect Science 16 36ndash43 httpsdoiorg101016jcois201605007

BoykinLMampDeBarroPJ(2014)Apracticalguidetoidentifyingmem-bersoftheBemisia tabacispeciescomplexAndothermorphologicallyidenticalspeciesFrontiers in Ecology and Evolution245

CareyJR(1993)Applied demography for biologists with special emphasis on insectsNewYorkNYOxfordUniversityPress

CasteelCLDeAlwisMBakADongHWhithamSAampJanderG (2015) Disruption of ethylene responses by Turnip mosaic virus mediatessuppressionofplantdefenseagainstthegreenpeachaphidvector Plant Physiology 169 209ndash218 httpsdoiorg101104pp1500332

F IGURE 6emspPopulationprojectionoftheB tabacibiotypeQonhealthyandToCV-infectedtomatoplantsAninitialpopulationof10eggswasusedineachprojection

8emsp |emsp emspensp LI et aL

ChenWHasegawaDKKaurNKliotAPinheiroPVLuanJhellipFeiZ(2016)ThedraftgenomeofwhiteflyBemisia tabaciMEAM1aglobalcroppestprovidesnovel insights intovirustransmissionhostadaptationand insecticide resistanceBMC Biology14110httpsdoiorg101186s12915-016-0321-y

Chi H (1988) Life-table analysis incorporating both sexes and variabledevelopment rates among individualsEnvironmental Entomology1726ndash34httpsdoiorg101093ee17126

ChiH(1990)Timingofcontrolbasedonthestagestructureofpestpop-ulationsA simulation approach Journal of Economic Entomology831143ndash1150httpsdoiorg101093jee8341143

Chi H (2016) TIMING-MSChart Computer program for population projection based on age-stage two-sex life table Retrieved fromhttp140120197173Ecology

Chi H (2017) TWOSEX-MSChart a computer program for age-stagetwo-sexlifetableanalysis

ChiHampLiuH(1985)Twonewmethodsforthestudyofinsectpopu-lationecologyBulletin of the Institute of Zoology Academia Sinica24225ndash240

ChiHamp SuHY (2006)Age-stage two-sex life tables ofAphidius gi-fuensis (Ashmead) (Hymenoptera Braconidae) and its host Myzus persicae (Sulzer) (Homoptera Aphididae) with mathematical proofof the relationship between female fecundity and the net repro-ductive rate Environmental Entomology 35 10ndash21 httpsdoiorg1016030046-225X-35110

ChuDHuXGaoXZhaoHNicholsRLampLiX(2012)Useofmito-chondrialcytochromeoxidaseIpolymerasechainreaction-restrictionfragmentlengthpolymorphismforidentifyingsubcladesofBemisia ta-baciMediterraneangroupJournal of Economic Entomology105242ndash251httpsdoiorg101603EC11039

ChuDZhangYJBrownJKCongBXuBYWuQJampGuoR (2006) The introduction of the exotic Q biotype of Bemisia ta-baci (Gennadius) from the Mediterranean region into China on or-namental crops Florida Entomologist 89 168ndash174 httpsdoiorg1016530015-4040(2006)89[168TIOTEQ]20CO2

DaiHJLiuYGZhuXPLiuYJampZhaoJ(2016)Tomato chlorosis virus(ToCV)transmittedbyBemisia tabacibiotypeQofShouguanginShandongProvinceJournal of Plant Protection43162ndash167

DeBarroPJLiuSSBoykinLMampDinsdaleAB(2011)Bemisia tabaciAstatementofspeciesstatusAnnual Review of Entomology561ndash19httpsdoiorg101146annurev-ento-112408-085504

DinsdaleACook LRiginosCBuckleyYMampDeBarroP (2010)Refined global analysis of Bemisia tabaci (Gennadius) (HemipteraSternorrhynchaAleyroidea)mitochondrialCOItoidentifyspecieslevelgeneticboundariesAnnals of the Entomological Society of America103196ndash208httpsdoiorg101603AN09061

DonaldsonJRampGrattonC(2007)Antagonisticeffectsofsoybeanvi-ruses on soybean aphid performanceEnvironmental Entomology36918ndash925httpsdoiorg101093ee364918

DovasCIKatisNIampAvgelisAD(2002)Multiplexdetectionofcrini-viruses associatedwith epidemics of a yellowing disease of tomatoin Greece Plant Disease 86 1345ndash1349 httpsdoiorg101094PDIS200286121345

EfronBampTibshiraniRJ(1993)An Introduction to the BootstrapNewYorkNYChapmanandHallhttpsdoiorg101007978-1-4899- 4541-9

FereresAPentildeaflorMFFavaroCFAzevedoKELandiCHMalutaNKhellipLopesJR(2016)Tomatoinfectionbywhitefly-transmittedcirculative and non-circulative viruses induce contrasting changesin plant volatiles and vector behaviour Viruses 8 225 httpsdoiorg103390v8080225

GoodmanD(1982)OptimallifehistoriesoptimalnotationandthevalueofreproductivevalueThe American Naturalist119803ndash823httpsdoiorg101086283956

HuangYBampChiH (2011)Theage-stage two-sex life tablewithanoffspringsexratiodependentonfemaleageJournal of Agriculture and Forestry60337ndash345

HuangYBampChiH(2012)AssessingtheapplicationoftheJackknifeandBootstraptechniquestotheestimationofthevariabilityofthenetre-productiverateandgrossreproductiverateAcasestudyinBactrocera cucurbitae (Coquillett) (DipteraTephritidae)Journal of Agriculture and Forestry6137ndash45

JiuMZhouXPTongLXuJYangXWanFHampLiuSS(2007)Vector-virus mutualism accelerates population increase of an inva-sive whitefly PLoS ONE 2 e182 httpsdoiorg101371journalpone0000182

Jones D R (2003) Plant viruses transmitted by whitefliesEuropean Journal of Plant Pathology 109 195ndash219 httpsdoiorg101023A1022846630513

LesliePH(1945)Ontheuseofmatricesincertainpopulationmathemat-icsBiometrika33183ndash212httpsdoiorg101093biomet333183

LewisEG(1942)OnthegenerationandgrowthofapopulationSankhya693ndash96

LiMLiuJampLiuSS (2011)Tomato yellow leaf curl virus infectionoftomatodoesnotaffecttheperformanceoftheQandZHJ2biotypesoftheviralvectorBemisia tabaci Insect Science1840ndash49httpsdoiorg1011112Fj1744-7917201001354x

LvJZSangPTLiLZampLiXD(2010)Effectofnutrientsolutionwithdifferent formulasandconcentrationsonthegrowthof tomatoseedlingJournal of Shanxi Agricultural University30112ndash116

MannRSSidhuJSButterNSSohiASampSekhonPS (2008)PerformanceofBemisia tabaci(HemipteraAleyrodidae)onhealthyandCotton leaf curl virusinfectedcottonFlorida Entomologist91249ndash255httpsdoiorg1016530015-4040(2008)91[249POBTHA]20CO2

MatsuuraSampHoshinoS(2009)EffectoftomatoyellowleafcurldiseaseonreproductionofBemisia tabaciQbiotype(HemipteraAleyrodidae)on tomato plants Applied Entomology and Zoology 44 143ndash148httpsdoiorg101303aez2009143

Navas-CastilloJFiallo-OliveEampSanchez-CamposS (2011)EmergingvirusdiseasestransmittedbywhitefliesAnnual Review of Phytopathology49219ndash248httpsdoiorg101146annurev-phyto-072910-095235

PanH ChuDGeDWang SWuQ XieWhellipZhangY (2011)Further spread of and domination by Bemisia tabaci (HemipteraAleyrodidae) biotypeQ on field crops in China Journal of Economic Entomology104978ndash985httpsdoiorg101603EC11009

Pan H Chu D Liu B Shi X Guo L XieW hellip Zhang Y (2013)Differential effects of an exotic plant virus on its two closely re-lated vectors Scientific Reports 3 2230 httpsdoiorg101038srep02230

PentildeaflorMFMauckKEAlvesKJDeMoraesCMampMescherMC(2016)EffectsofsingleandmixedinfectionsofBean pod mottle virus and Soybean mosaic virusonhost-plantchemistryandhost-vectorinteractionsFunctional Ecology301648ndash1659

Polat-AkkoumlpruumlEAtlihanROkutHampChiH(2015)Demographicas-sessmentofplantcultivarresistancetoinsectpestsacasestudyofthedusky-veinedwalnutaphid(HemipteraCallaphididae)onfivewalnutcultivars Journal of Economic Entomology108 378ndash387 httpsdoiorg101093jeetov011

PolstonJEDeBarroPampBoykinLM(2014)TransmissionspecificitiesofplantviruseswiththenewlyidentifiedspeciesoftheBemisia tabaci species complex Pest Management Science70 1547ndash1552 httpsdoiorg1010022Fps3738

RaoQLuoCZhangHGuoXampDevineGJ(2011)DistributionanddynamicsofBemisia tabaciinvasivebiotypesincentralChinaBulletin of Entomological Research 101 81ndash88 httpsdoiorg101017S0007485310000428

ReddyGVampChiH (2015)Demographiccomparisonofsweetpotatoweevil reared on a major host Ipomoea batatas and an alternative

emspensp emsp | emsp9LI et aL

host I triloba Scientific Reports 5 11871 httpsdoiorg101038srep11871

RubinsteinGampCzosnekH(1997)Long-termassociationoftomato yellow leaf curl viruswithitswhiteflyvectorBemisia tabaciEffectontheinsecttransmissioncapacitylongevityandfecundityJournal of General Virology782683ndash2689httpsdoiorg1010990022-1317-78-10-2683

SaskaPSkuhrovecJLukaacutešJChiHTuanSJampHoněkA (2016)Treatmentbyglyphosate-basedherbicidealterslifehistoryparametersoftherose-grainaphidMetopolophium dirhodum Scientific Reports627801httpsdoiorg101038srep27801

SidhuJSMannRSampButterNS(2009)DeleteriouseffectsofCotton leaf curl virus on longevity and fecundity of whitefly Bemisia tabaci (Gennadius)Journal of Economic Entomology662ndash66

StoutMJThalerJSampThommaBP(2006)Plant-mediatedinterac-tionsbetweenpathogenicmicroorganismsandherbivorousarthropodsAnnual Review of Entomology51 663ndash689 httpsdoiorg101146annurevento51110104151117

SuQPreisserELZhouXXieWLiuBMWangSLhellipZhangY J (2015) Manipulation of host quality and defense by a plantvirus improves performance ofwhitefly vectors Journal of Economic Entomology10811ndash19httpsdoiorg101093jeetou012

TsaiW S Shih S LGreen SKampHanson P (2004) First report ofthe occurrence of Tomato chlorosis virus and Tomato infectious chlo-rosis virus in Taiwan Plant Disease88 311httpsdoiorg101094PDIS2004883311B

Tuan SJ LeeCCampChiH (2014a) Population anddamagepro-jection of Spodoptera litura (F) on peanuts (Arachis hypogaea L)under different conditions using the age-stage two-sex life tablePest Management Science 70 805ndash813 httpsdoiorg101002ps3618

TuanSJLeeCCampChiH(2014b)Populationanddamageprojec-tion ofSpodoptera litura (F) on peanuts (Arachis hypogaea L) underdifferent conditions using the age-stage two-sex life table Pest Management Science701936httpsdoiorg101002ps3920

TzanetakisIEMartinRRampWintermantelWM(2013)Epidemiologyofcrinivirusesanemergingproblem inworldagricultureFrontiers in Microbiology4119

Wang Z RWang X XDuY CGao J CGuoYMampHuang ZJ (2016) Research progress on Tomato chlorosis virus disease Acta Horticulturae Sinica431735ndash1742

WintermantelWMCorteaAAAnchietaAGGulati-SakhujaAampHladkyLL(2008)Co-infectionbytwocrinivirusesaltersaccumula-tionofeachvirusinahost-specificmannerandinfluencesefficiencyof virus transmission Phytopathology 98 1340ndash1345 httpsdoiorg101094PHYTO-98-12-1340

WintermantelWMampWislerGC(2006)VectorspecificityhostrangeandgeneticdiversityofTomato chlorosis virus Plant Disease90814ndash819httpsdoiorg101094PD-90-0814

XuHXHeXCZhengXSYangYJampLuZX(2014)InfluenceofRice black streaked dwarf virusontheecologicalfitnessofnon-vectorplanthopper Nilaparvata lugens (Hemiptera Delphacidae) Insect Science21507ndash514httpsdoiorg1011111744-791712045

YinJSunYWuGampGeF(2010)EffectsofelevatedCO2associatedwithmaizeonmultiplegenerationsofthecottonbollwormHelicoverpa armigera Entomologia Experimentalis et Applicata13612ndash20httpsdoiorg101111j1570-7458201000998x

ZhengXMTaoYLChiHWanFHampChuD(2017)Adaptabilityofsmallbrownplanthopper to four ricecultivarsusing life tableandpopulationprojectionmethodScientific Reports742399httpsdoiorg101038srep42399

SUPPORTING INFORMATION

Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle

How to cite this articleLiJDingTBChiHChuDEffectsofTomato chlorosis virusontheperformanceofitskeyvectorBemisia tabaciinChinaJ Appl Entomol 2017001ndash9 httpsdoiorg101111jen12477