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Can Cities Activate Sleeper Species and Predict Future Forest Pests? A Case Study of Scale Insects

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Sleeper species are innocuous native or naturalized species that exhibit invasive characteristics and become pests in response to environmental change. Climate warming is expected to increase arthropod damage in forests, in part, by transforming innocuous herbivores into severe pests: awakening sleeper species. Urban areas are warmer than natural areas due to the urban heat island effect and so the trees and pests in cities already experience temperatures predicted to occur in 50-100 years. We posit that arthropod species that become pests of urban trees are those that benefit from warming and thus should be monitored as potential sleeper species in forests. We illustrate this with two case studies of scale insects that are important pests of urban trees in parts of the US. Melanaspis tenebricosa and Parthenolecanium quercifex are geographically native to the US but take on invasive characteristics such as higher survival and reproduction and become disconnected from natural enemies on urban trees due to the urban heat island effect. This allows them to reach high densities and damage their host trees. Parthenolecanium quercifex density increases up to 12 times on urban willow oaks with just 2 °C of warming due to higher survival and adaptation to warmer temperatures. The urban heat island effect also creates a phenological mismatch between P. quercifex and its parasitoid complex, and so egg production is higher. Melanaspis tenebricosa density can increase 300 times on urban red maples with 2.5 °C of warming. This too is due to direct effects of warmer temperatures on survival and fecundity but M. tenebricosa also benefits from the drought stress incurred by warmer urban trees. These effects combine to increase M. tenebricosa density in forests as well as on urban trees at latitudes higher than its native range. We illustrate how cities provide a unique opportunity to study the complex effects of warming on insect herbivores. Studying pestilent urban species could be a pragmatic approach for identifying and preparing for sleeper species.
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Insects2020,11,142;doi:10.3390/insects11030142www.mdpi.com/journal/insects
Article
CanCitiesActivateSleeperSpeciesandPredict
FutureForestPests?ACaseStudyofScaleInsects
StevenD.Frank*andMichaelG.Just
DepartmentofEntomologyandPlantPathology,CampusBox7613,NorthCarolinaStateUniversity,
Raleigh,NC27695,USA;mjust@ncsu.edu
*Correspondence:sdfrank@ncsu.edu
Received:10January2020;Accepted:19February2020;Published:25February2020
Abstract:Sleeperspeciesareinnocuousnativeornaturalizedspeciesthatexhibitinvasive
characteristicsandbecomepestsinresponsetoenvironmentalchange.Climatewarmingisexpected
toincreasearthropoddamageinforests,inpart,bytransforminginnocuousherbivoresintosevere
pests:awakeningsleeperspecies.Urbanareasarewarmerthannaturalareasduetotheurbanheat
islandeffectandsothetreesandpestsincitiesalreadyexperiencetemperaturespredictedtooccur
in50–100years.Wepositthatarthropodspeciesthatbecomepestsofurbantreesarethosethat
benefitfromwarmingandthusshouldbemonitoredaspotentialsleeperspeciesinforests.We
illustratethiswithtwocasestudiesofscaleinsectsthatareimportantpestsofurbantreesinparts
oftheUS.MelanaspistenebricosaandParthenolecaniumquercifexaregeographicallynativetotheUS
buttakeoninvasivecharacteristicssuchashighersurvivalandreproductionandbecome
disconnectedfromnaturalenemiesonurbantreesduetotheurbanheatislandeffect.Thisallows
themtoreachhighdensitiesanddamagetheirhosttrees.Parthenolecaniumquercifexdensity
increasesupto12timesonurbanwillowoakswithjust2°Cofwarmingduetohighersurvivaland
adaptationtowarmertemperatures.Theurbanheatislandeffectalsocreatesaphenological
mismatchbetweenP.quercifexanditsparasitoidcomplex,andsoeggproductionishigher.
Melanaspistenebricosadensitycanincrease300timesonurbanredmapleswith2.5°Cofwarming.
ThistooisduetodirecteffectsofwarmertemperaturesonsurvivalandfecunditybutM.tenebricosa
alsobenefitsfromthedroughtstressincurredbywarmerurbantrees.Theseeffectscombineto
increaseM.tenebricosadensityinforestsaswellasonurbantreesatlatitudeshigherthanitsnative
range.Weillustratehowcitiesprovideauniqueopportunitytostudythecomplexeffectsof
warmingoninsectherbivores.Studyingpestilenturbanspeciescouldbeapragmaticapproachfor
identifyingandpreparingforsleeperspecies.
Keywords:globalchange;latentinvasivespecies;urban;warming
Sleeperspeciesareinnocuousnativeornaturalizedspeciesthatexhibitinvasivecharacteristics
andbecomepestsinresponsetoenvironmentalchange[1].Climatewarmingisexpectedtoincrease
arthropoddamageinforests,inpart,bytransforminginnocuousherbivoresintoseverepests:
awakeningsleeperspecies[2–4].Severalnativeinsectherbivoreshavealreadybecomeinvasiveforest
pests.Forexample,warminghastransformedthemountainpinebeetle(Dendroctonusponderosae
(Hopkins))fromanintermittentoutbreakpesttoaninvasivepestbyincreasingwintersurvival,
voltinism,andgeographicrange(latitudeandaltitude)[5–8].Inthesenewlyinvadedareas,mountain
pinebeetlesencounterednaivehosttrees,oftenstressedbyclimate,amplifyingtheirlethality[9,10].
Southernpinebeetle(DendroctonusfrontalisZimmermann),nativetothesouthernUS,andpine
processionarymoth(ThaumetopoeapityocampaDenisandSchiffermüller),nativetotheMediterranean
region,havealsospreadandbecomedamagingpestsaswarmerwintershavepermittedtheir
Insects2020,11,1422of16
survivalathigherlatitudes[11,12].Treeshostaremarkablenumberofherbivorousarthropod
species.Forexample,QuercusandAcertreesinthemidAtlanticUSAhost535and297Lepidoptera
species,respectively[13].IntheBritishIsles,Quercustreeshostover400insectspecies[14].Withso
manynativeornaturalizedinsectspeciesonagiventreeandcontinuedwarming,howdoweidentify
andprepareforsleeperspecies?
Citiesarewarmerthanadjacentnaturalareasduetotheurbanheatisland(UHI)effect[15].
Urbantreesliveatthesewarmertemperaturesandoftenhavemorearthropodpeststhantreesin
naturalareas[16–19].TheUHIeffectcanincreaseherbivorepopulationsdirectlybyincreasingtheir
developmentrate,voltinism,wintersurvival,orfecundity[18,20–23].TheUHIeffectcanincrease
herbivorepopulationsindirectlybyincreasinghostplantqualityorreducingregulationbynatural
enemies[18,20].Warmertemperaturesarenottheonlyreasonbackgroundherbivoresbecome
invasivepestsonurbanplantsbuttheUHIeffectisamajordriverstructuringarthropodcommunities
[24–28].Citiesprovideopportunitiestostudythecomplexeffectsofwarmingnow,evenwhen
consideringforenvironmentaldifferences,suchaslandcover,disturbance,soilmoisture,andnatural
enemies,betweencitiesandnaturalhabitats(asreviewedin[29]).Thus,citiesmayhelppredictthe
responseofplantsandanimalstoclimatechange[29].Pestiferousspeciesthatthriveonurbantrees
maybesleeperspeciesthatwillbecomeinvasiveforestpestswithcontinuedwarming.
Invasivespeciesoftenhaveinherentorplastictraitsthatincreasetheirfitness,competitiveness,
orreproductiverateascomparedtononinvasivespecies[30–32].Thereisnosetdefinitionofwhat
characteristicsmakeaspeciesinvasive,butratheracollectionofcharacteristicsthatarecommonto
speciesconsideredinvasive.Thesecharacteristicsareusuallyappliedtononnativespeciesand
includesexualandasexualreproduction,highreproductiveanddispersalrates,phenotypicplasticity
oradaptation,releasefromenemies,rapidgeographicspread,andnegativeeffectsonhuman
interestsandbiodiversity[33–38].Warmingcanpromoteoractivatethesetraitsinsomeherbivorous
arthropods[34,39,40].Forexample,thediamondbackmoth(Plutellaxylostella(L.))isalongdistance
disperserandisacosmopolitanagriculturepest[41].Climatewarminghasincreaseditsdispersal
abilityaswarmeraircurrentsfacilitatelongerdistancedispersal,allowingittobepestilentinareas
whereitcouldnotsuccessfullyoverwinter[42,43],thoughestablishmentisoccurringinsomeofthese
areasastheybecomewarmer[44].Withwarming,theeasternlarchbeetle(DendroctonussimplexLe
Conte)hasbecomemorepestilentinitsnativerange[45],withsomepopulationschangingfrom
univoltinetobivoltineduringwarmeryears[46].Speciesthatdisplayinvasivephenotypes(i.e.,those
phenotypesthatincludecharacteristicsconsideredinvasive)duetourbanwarmingmaybethe
sleeperspeciesthatwillbecomeinvasiveforestspestswithcontinuedclimatewarminge.g.,[47,48].
Theeffectsofurbanwarminghavebeenparticularlywellstudiedfortwoscaleinsecttaxathat
areurbantreepests,gloomyscale,Melanaspistenebricosa(Comstock)andoaklecaniumscale
Parthenolecaniumquercifex(Fitch).Thesescalespeciesdevelopinvasivetraits,proliferate,andbecome
chronicurbantreepestsduetotheUHIeffect[49–51].Otherscalespeciesonthesametreesunder
thesameconditionsdonotdisplayinvasivephenotypesorbecomepests[52,53].Melanaspis
tenebricosaandP.quercifexareconsistentwithcharacterizationsofsleeperspeciesastheyare
innocuousnativespeciesthatbecomepestswithenvironmentalchange,here,theUHIeffect.
Moreover,wesuspectthatactivationofthesespeciesandotherspeciesbytheUHIeffectforewarns
theiremergenceasforestpestsastheclimatewarms.Here,wepresentcasestudiesofthesescale
insectspeciestodescribehowtheyhavebecomeinvasiveincitiesandhowthesecharacteristicscould
predicttheireventualemergenceasforestpests.Wefocusonafewtraitsassociatedwithinvasive
speciesthatcouldbeandhavebeenaffectedbywarming:(1)phenotypicplasticitythatincreases
fitnessandabundance,(2)theuncouplingofinteractionswithlocalnaturalenemies,and(3)
geographicrangeexpansion(Table1).Wereviewresearchonthesespeciesanddemonstratethe
primacyofwarminginalteringthesetraits—leadingtohighdensitiesandvirulenceofthesepests—
ascomparedtootherenvironmentalfactors.Wealsodiscussevidencefortheirpotentialtospread
intonaturalforestswithclimatewarmingandhowthisapproachcouldbeusedmoregenerally.
Table1.Summaryoftheeffectsofurbanwarmingongloomyscale(Melanaspistenebricosa)andoak
lecaniumscale(Parthenolecaniumquercifex)invasiveness.
Insects2020,11,1423of16
InvasiveTraitM.tenebricosa P.quercifex
Increased
reproductiverate
Greaterembryoproductiononwarmer
trees[21]
Greaterovisacdensityonwarmertrees
[54]
Increaseddensity
Scaledensity200timesgreateron
urbantreeswith2.5°Cofwarming
[55];
Scaledensity8–12timesgreateronurban
treeswith2.5°Cofwarming[54];
fivetimesmoreabundantonstreet
treesthanforesttrees[56];greater
accumulation[50]
seventimesmoreabundantatlowthan
highlatitudesandonstreetthanforest
trees(Δ3.8°Clatitude)[57]
Plasticorgenetic
adaptation/phenot
ypicchange
Scalesare30%largeronwarmerurban
trees[21];greatersurvival[21,58];
greaterestablishment[50,58]
Crawlersurvival20%greaterathigher
temperatures[58,59];threetimesgreater
density[58,59];threetimesgreater
densityinwarmedcommongarden[57]
Enemyrelease
Noincreaseintotalnaturalenemy
density[21]orparasitoiddensity[56]
withurbanwarmingornaturalenemy
densitytracksscaledensity[56]
Phenologicalmismatchbetweenscales
andparasitoidsonwarmurbantrees[51]
RangeexpansionNorthwardexpansion[57,60];foundat
greaterelevations[61]noobservationsavailable
1.OakLecaniumScaleandWillowOaks
Naturalhistory.ParthenolecaniumquercifexisnativetotheeasternUSandfeedsprimarilyonoak
trees(Figure1).Theyfeedonphloemfromleavesorbranchesdependingontheirlifestage.
Parthenolecaniumquercifexareunivoltineandadultfemalesbeginovipositioninlatespring[62].
Duringthisperiod,thefemaleswellsandarcheshertesttoproduceahemisphericalcontainerforthe
eggs(i.e.,ovisac).Parthenolecaniumquercifexproduceupto3000eggsoveraperiodofapproximately
4weeks.Eggstypicallyhatchwithinaweek.Crawlers(i.e.,firstinstars)migratefromovisacsto
leaveswheretheyfeedthroughsummer.Infall,theymolttosecondinstarsandmigratebacktotree
stems.Parthenolecaniumquercifexoverwinterassecondinstarsanddevelopintoadultsinearlyspring.
Insects2020,11,1424of16
Figure1.Willowoak(Quercusphellos)branchheavilyinfestedwithoaklecaniumscale
(Parthenolecaniumquercifex)ovisacs.Photo:ClydeSorenson,NorthCarolinaStateUniversity.
Parthenolecaniumquercifexfeedsonmanyoakspecies[63]butisaprimarypestofwillowoak
treesintheeasternUS[49].ThenativedistributionofwillowoaksineasternUSforestsisfromNew
JerseytonorthernFloridaandtheyareamongthemostplantedtreesinUScitiesthroughoutthe
southeasternandmidAtlanticstates[64].Willowoakshostdiversearthropodcommunities,
includingmanyspecialistandgeneralistherbivores[63].Amongtheseareatleast12scalespecies
andmanyotherrelatedhemipterans,includingthecongener,Parthenolecaniumcorni,whichisnot
nativetotheUSbutoftencooccurswithP.quercifexonurbantrees.Thespeciesareindistinguishable
duringallbutthefirstinstar[65].Therefore,researchhasoftenreportedtheircombinedabundance.
SevereinfestationsofP.quercifexcanreducetreegrowthespeciallywhencombinedwithother
stressorslikedrought[59].Parthenolecaniumquercifexalsoproducehoneydewthatcoatsleavesand
othersurfacesandisasubstrateforsootymolds.
Relationshipofwarminganddensity.Parthenolecaniumquercifexdensityisgenerallygreateron
urbanwillowoaksthanwillowoaksinforests.TherelationshipbetweenP.quercifexdensityand
temperaturehasbeenexploredwithobservationalandmanipulativeexperiments.Inoneexperiment,
ageoreferencedurbantreedatabaseandLandsatsurfacetemperaturedatawereusedtoselectwillow
oakstreettreesfromthewarmestandcoolestlocationsinRaleigh,NC,US(35°4715.8N,78°3839.3
W)[54].Temperaturewasalsorecordedthroughouttheexperimentwithinsitudataloggers.Scale
densitywasrecordedthroughouttheyeartoassessdensityatdifferentlifestages:ovisacsinspring,
firstinstarsonleavesinsummer,andsecondinstarsontwigsinfall.Thedensityofeachlifestage
was8–12timeshigheronthewarmtreesthancooltrees[54].Nodifferenceswerefoundinnatural
enemyabundanceorpercentparasitismofadults,suggestinganimportantroleoftemperatureon
scaledensity.Similarobservationalexperimentsusingstreettreesproducedcomparable
relationshipsbetweentemperatureandP.quercifexdensityandnaturalenemies[51,59].Willowoaks,
Insects2020,11,1425of16
andotheroakspecies,hostotherscalespecies[49,63],butonlyP.quercifexdensityincreasedwith
temperatureinthisstudy.
TherelationshipbetweenP.quercifexdensityandtemperaturewasfurtherconfirmedwith
experimentscomparingstreettreestoforesttreesatthesameanddifferentlatitudes[57].Scale
density,temperature,andnaturalenemycommunitywererecordedforstreettreesinRaleighand
3.8degreesoflatitudehigherinNewark,DE,US(39°411.4N,75°4458.8W).Meancanopy
temperatureofstreettreesinRaleighwas0.8°Cwarmerthanthatofforesttreesandstreettreeshad
overeighttimesmoreP.quercifex.Newarkhadameantemperatureduringtheobservationalperiod
3.1°CbelowthatofRaleigh,similartothedifferencebetweenRaleighstreetandforesttrees.Overall,
NewarktreeshadseventimeslessscalesthanRaleighstreettrees,similartothedifferencesbetween
Raleighstreetandforesttrees.TherewerenoscalesdetectedonforesttreesinNewark.Thissuggests
thatthecoolerbackgroundtemperatureofNewark,duetolatitude,limitedP.quercifexfromreaching
pestdensitiesonurbantreesandthattherecouldbeathresholdtemperatureatwhichP.quercifex
switchfrombackgroundtopestiferousherbivores[57].Themechanismsdrivingthischangein
densityneedtobeuncoveredbecausetheyareimportantforunderstandingtheactivationofsleeper
speciesandpotentialforscalestoreachhighdensitiesinlocationsthatarecurrentlyatlowdensities.
Invasivetrait:phenotypicchange.Highsurvivalrateisamechanismthatincreasesthepopulation
growth,spread,andpersistenceofinvasivespecies[66].Growthchamberexperimentswere
conductedtodeterminewhethergreatersurvivalisamechanismforP.quercifexdensityontrees
underwarmconditions[59].Greenhouseandgrowthchamberexperimentshelpcontrolfor
potentiallyconfoundingbioticandabioticfactorsthatmaydifferbetweenurbanandnaturalareas,
suchassoiltype,plantcover,naturalenemypresenceandactivity,wateravailability,andpollutants.
Parthenolecaniumquercifexovisacscollectedfromurbantreeswereattachedtowillowoaksaplingsin
largegrowthchambers(9m3).Saplingsweregrownineitherwarmorcoolchambersunderhighor
lowwatertreatments.Thecoolchambertemperaturewassettothemonthlymeanoutdoor
temperature(30yearnormals)[67].Thewarmchamberwasmaintainedat4°Chigherthanaverage
toemulatetheUHIeffect.Firstinstarscaleshadapproximately20%greatersurvivalinthemonth
aftereclosioninthewarmchambersthancoolchambers.Waterstressdidnothaveasignificanteffect
onP.quercifexsurvival[59].Crawlersarethemostvulnerablestageofscaleinsectsandtheirsurvival
isoftenlow.Thus,greatersurvivalduringthisimportantlifestagecouldaffectpopulationgrowthin
fieldpopulations.
Scaleinsectscanadapttonewhostsorabioticconditionsthroughgeneticorplasticphenotypic
changesthatincreasetheirfitness[68–71].Agreenhouseexperimentwasconductedtodetermine
whetherP.quercifexcollectedfromwarmtreeswereadaptedto,andgainedanadvantagein,warmer
conditionsabsentotherurbanenvironmentalcharacteristics[54].Inthisexperiment,willowoak
saplingsweregrowninawarmgreenhousemaintainedat36/32°C(day/night)andinacool
greenhousethatwas32/28°C.Parthenolecaniumquercifexovisacswerecollectedfromtreesinwarm
andcoollocationsinRaleighandattachedtochambersaplingsinafactorialdesignthatincluded
scalethermalorigin(warmorcool)withchambertemperature(warmorcool).Afterthreemonths,
thedensityofscalesfromovisacsfromcooltreeswassimilarinwarmandcoolchambers.Thedensity
ofscalesfromovisacsfromwarmtreeswasoverthreetimesgreaterinwarmchambersthanincool
chambers.Thissuggestsscalesfromwarmtreeshadsomeplasticorgeneticadaptationtowarmer
conditionsthatincreasedtheirsurvivalanddensities.Warmingscalesfromcooltreesdidnot
producetheinvasivephenotype(i.e.,survivalwasnotgreater)inthesingleseasonoftheexperiment
[54].Multigenerationexperimentsareneededtodeterminewhetherscalesacquirethisphenotype
throughmaternaleffectsorothermechanisms.
Thehypothesisthatscalesincoolclimatesdevelopinvasivephenotypeswithclimatewarming
canbetestedwithreciprocaltransplantandcommongardenexperimentsthatalsohelpalleviatethe
confoundingeffectsofnontemperatureurbanconditionsonscaleresponses.Acommongarden
experimentwasconductedtohelpdeterminewhetherP.quercifexathighlatitudescoulddevelop
invasivephenotypesthatincludedhighersurvivalanddensityastheclimatewarmed[57].
ParthenolecaniumquercifexovisacswerecollectedfromNewark,DEandfromRaleigh,NCinspring
Insects2020,11,1426of16
andthenattachedtoyoungwillowoaksplantedinacommongardeninRaleigh.Raleighhasamean
temperaturethatisapproximately2.8°CwarmerthanNewark.Thus,thisdesignsimulatedglobal
estimatesofclimatewarmingoverthenext50–100years[72].ScalesfromNewarkreacheddensities
morethanthreetimesgreaterthanscalesfromRaleighandthesedensitiesarenotoftenrecorded
fromurbantreesinNewark[57].ThissuggeststhatclimatewarmingcouldactivateP.quercifex
throughmechanismssuchasincreasedsize,fecundity,orsurvival—inareaswhereitcurrentlyexists
asabackgroundherbivore.
Invasivetrait:uncouplednaturalenemyinteractions.Manynativeandexoticspeciesbecome
invasivebecausetheyareuncoupledfromnaturalenemies[73].Climatewarmingcanalsodisrupt
trophicinteractionsbychangingnaturalenemybehavior,abundance,orcommunitycomposition
[74–77].Warmingcanalsocreatephenologicalmismatchesbetweenherbivoresandnaturalenemies
whicharepredictedtooccurfrequentlywithclimatewarming[78–80].
FieldresearchonP.quercifexhasshownthatitsnaturalenemycommunitiesaresimilarbetween
treesinwarmandcoolareasaswellasbetweenforestandstreettrees[54,57].Infact,naturalenemies,
likeparasitoids,areoftenmoreabundantintreeswithmorescales[19,21,81].Percentparasitismof
P.quercifex,assessedbydissections,wasalsosimilarbetweenscalesonwarmandcoolstreettreesin
Raleigh[54].Takentogetherthisevidencesuggeststhatwarmingincreasedscaledensitydirectly,as
discussedabove,ratherthanindirectlybyalteringinteractionswithnaturalenemies.However,a
fieldexperimentuncoveredaphenologicalmismatchbetweenP.quercifexandparasitoidsatakey
stageinitslifecyclethatcontributedtogreaterreproductivesuccessandpopulationgrowth[51].
Parthenolecaniumquercifexproduceeggsinspringandaroundthetimeofoviposition,several
parasitoidsbecomeactiveandparasitizetheadultfemalescalesandlayeggsthatdevelopwithinthe
scalebodyorovisac[82].Parasitismcanreduceorpreventovipositiondependingwhenitoccurs
duringdevelopment.Inthisfieldexperiment,femalescalesfromstreettreesinwarmsitesandsites
approximately2.5°Ccoolerwerecollectedweekly,startingpriortooviposition.Ateachcollection,
theproportionofeggproducingscalesandtheproportionofparasitizedscaleswasrecorded.Scales
onwarmtreesproducedeggsapproximatelytwoweeksearlierthanscalesoncooltrees.Scaleswere
parasitizedatsimilarratesonwarmandcooltreesbutscalesonwarmtreesproducedmoreeggs
beforetheywereparasitized.Thus,eggproductionbyunparasitizedscaleswassimilaronwarmand
cooltreesbuteggproductionwasdoubledforparasitizedscalesinwarmtrees[51].Greateregg
productionduetothismismatchcoupledwithhighersurvivaloffirstinstarsonwarmtreescould
increasepopulationgrowth,aninvasivetrait,and,thus,makeP.quercifexaninvasivespecies.
2.GloomyScaleandRedMaples
Naturalhistory.Gloomyscale,Melanaspistenebricosa,isnativetothesoutheasternUS(Figure2).
Itfeedsprimarilyonredmapleandothermaplesthoughitcanbefoundonotherspecies,including
tulippoplar(Liriodendrontulipifera),hackberry(Celtisoccidentalis),sweetgum(Liquidambarstyraciflua),
andholly(Ilexamericana)[16,83].Melanaspistenebricosaisunivoltineandlivesontreebarkwhereit
feedsonfluidfromxylemorparenchymacells[84].Matedfemalesoverwinterandbeginoviposition
inlatespring.Eachscaleproducesupto5–7eggsperdayover6–8weeks[21,85].Crawlers(i.e.,first
instars)leavethetestandsettleonbranchesorthetrunk,oftenwithinafewcentimetersofthemother.
Atthesesettlingsites,acrawlermolts,buildsitstest,moltsagain,andexpandsitstest.Afterthelast
moltinlatesummer,wingedmalesemergetomatewithfemales—afterwhich,themalesdie[83].
Insects2020,11,1427of16
Figure2.Redmaple(Acerrubrum)branchheavilyinfestwithgloomyscale(Melanaspistenebricosa).
Photo:ElsaYoungsteadt,NorthCarolinaStateUniversity.Thesmallbumpscoveringthebarkare
scaletests.SeeDale,A.G.,Frank,S.D.,2014.UrbanWarmingTrumpsHerbivoreEnemies.Bull.Ecol.
Soc.Am.95,252–256foradditionalimages.
InthesoutheasternUS,M.tenebricosaareprimarilyapestofplantedredmaplesalongstreets
andinurbanlandscapes.Theywereidentifiedasthemostimportantpestofurbanredmaplesin
1912[16]andremainsotoday[49].Yet,redmaplesarehoststospecialistherbivoressuchaspainted
mapleaphids(Drepanaphisacerifoliae(Thomas))andmaplespidermites(Oligonychusaceris(Shimer)),
generalistherbivores,andatleast16otherscalespecies[63,84,86].InthesoutheasternUS,theseother
herbivoresrarelybecomechronicpestsofredmaplesinurbanorruralforests.Melanaspistenebricosa
densitiesincreaserapidlyonstreettrees6to10yearsafterplanting[50].Theycanreachdensities
exceeding70scalespercm[87]andencrustbranchesandtrunks,givingtreesadarkgray‘gloomy’
appearance.HeavyM.tenebricosainfestationscausediebackofsmallbranchesandsparsecanopies.
Eventually,largerbranchesmaydiewithtreesacquiringgenerallypoorconditionandappearance
[55].
Relationshipofwarminganddensity.Melanaspistenebricosadensityisgenerallygreateronurban
treesthantreesinnaturalareas[16,56,87].Gloomyscaledensityispositivelycorrelatedwithair
temperatureandtheamountofimpervioussurfacecoveraroundtrees[55].Initialresearchto
understandM.tenebricosainfestationofurbantreesassessedscaleandnaturalenemydensityand
communitycompositionontreesthatvariedincanopytemperatureandtheamountofcircumjacent
impervioussurfaceovertwoyears.Thetreesspannedatemperaturegradientofapproximately2.5
°Casmeasuredwithintheircanopies.Naturalenemydensityandcommunitycompositiondidnot
differamongthetreesandwerenotasignificantpredictorofscaledensityinpathanalyses[21].The
strongestpathindicatedthatimpervioussurfacecoverincreasedtemperaturewhich,inturn,
increasedscaledensity.Subsequentresearchonurbanredmaplescorroboratedtheseresults
[53,56,61,87].
ThebenefitsofwarmingforM.tenebricosawerealsoassessedbycomparingurbanandforest
treesinRaleighand3.8degreesoflatitudehigherinNewark,DE[56].Melanaspistenebricosadensity
wasmeasuredonsolitarytreesplantedinlandscapesandontreesgrowingnaturallyontheedgeand
interiorofadjacentforests.InRaleigh,landscapetreeswere1.5°Cwarmerthanforestedgeorinterior
treesandhadthreeordersofmagnitudemorescales.InNewark,whichhasameantemperaturethat
is2.8°CcoolerthanRaleigh,forestandlandscapetreeshadsimilar,lowscaledensitiesascompared
toRaleighstreettrees.Toseparatetheeffectsoftemperaturefromdifferencesinedaphicconditions
(e.g.,wateravailability,compaction,nutrients),anexperimentwasconductedwithpottedredmaple
saplings.Saplingswereplantedinbarkandsandpottingmixandinfestedwithgloomyscales.The
followingyearthepottedtreeswereplacednexttoasubsetofthelandscapeandforesttreesinlate
Insects2020,11,1428of16
spring(May2014)beforetheM.tenebricosaovipositionperiodandmovedtonurserypadafter
ovipositionended(July2014).Pottedtreeswerewateredthreetimeseachweek.Attheendofthe
secondsummer(September2016),scaledensitywasfivetimesgreateronpottedtreesnextto
landscapetreesthanonforesttrees,indicatingabenefitofthehighertemperatureinlandscapes.
Additionally,parasitoidandpredatorabundanceswerefourtimesgreaterinlandscapessuggesting
naturalenemieswerenotresponsibleforlowerM.tenebricosadensityinforests[56].
Invasivetrait:phenotypicchange.Commonphenotypicchangesobservedininvasivespeciesare
greatersizeorfecundity[88–90].Thesechangescanbeduetofavorableabioticconditions,higher
qualityfood,lesscompetition,orotherfactors[66,91–93].Inanobservationalexperiment,M.
tenebricosawerecollectedfromurbantreesthatspannedatemperaturegradientofapproximately2.5
°C[21].Thenumberofembryoswithinscaleswaspositivelycorrelatedwithtreecanopytemperature
ineachoffourcollectionsthatwereeachapproximatelyaweekapart.Scalesize(i.e.,bodylength)
wasalsopositivelycorrelatedtotemperatureinthisexperimentandscaleswereupto30%largerin
treesfromwarmerlocations.
Treequalityforherbivorescanincreaseordecreasewithwaterstressandtheeffectsofwater
stressonscaleshasbeenequivocal.Researchonwhitepeachscale(Pseudaulacaspispentagona
(Targioni))foundwaterstressreducedpopulationgrowthandsurvival[94].However,elongate
hemlockscales(FioriniaexternaFerris)becamemoreabundantontreessubjectedtowaterstress[95].
SomeresearchonM.tenebricosafoundthatalthoughscaledensitywaspositivelycorrelatedwith
canopytemperature,impervioussurfacecoverwasastrongerpredictorofscaledensity[96].
Impervioussurfacecoveraffectstemperaturebutalsothesoilmoistureavailabletotrees[97].As
such,treewaterstress,measuredasxylemwaterpotential,wasfoundtobecorrelatedwith
impervioussurfacecoveraroundredmaplesinadifferentstudy[55].
Afieldexperimentwasconductedtodisentangletheeffectsoftemperatureandwaterstresson
M.tenebricosadensityandfecundity[98].Pairsofredmaplestreettreeswereselectedat30sitesin
Raleighthatspannedarangeofimpervioussurfacecoverandairtemperature.Onetreeineachpair
wasassignedtoa‘watered’treatmentandreceivedsupplementalwaterthroughthesummerfortwo
years,‘unwatered’treesreceivednosupplementalwater.Thus,thetemperaturewhichincreaseswith
impervioussurfacecouldbeseparatedfromwaterstresswhichalsoincreaseswithimpervious
surface.Slowreleaseirrigationbagswereplacedoneachtreeinthewateredtreatmentandfilled
twiceeachweekfromJunethroughAugust,whentemperatureandwaterstressaregreatestin
Raleigh,NC.Melanaspistenebricosafecunditywasmeasuredafteratwoyearexperimentalduration.
Therewereadditivemaineffectsoftemperatureandwateringinwhichthewarmestunwateredtrees
hadapproximately17%moreembryosthanwarmwateredtreesbutthesehad65%morethancool
wateredtrees[98].Thus,highertemperatureandtreewaterstress,bothofwhichwillincreasewith
climatechange,workinconcerttoproducetheinvasivephenotypesofhigherfecundityand
populationgrowth.
Melanaspistenebricosasurvivalandestablishmentalsoincreasesatwarmertemperatures.The
proportionofscalesthatsurvivedfromoneyeartothenextwasgreaterontreesthatwere2.5°C
warmerthancoolertreesinRaleigh,NCasmeasuredbytheratioofadultsfromonegenerationto
thenext[21].Inanotherstudy,M.tenebricosaestablishmentandrateofscaleaccumulationwas
greaterontreessurroundedbygreaterproportionsofimpervioussurface[50].Agrowthchamber
experimentwasusedtotesttheeffectoftemperature,whilelimitingorremovingtheeffectofother
uniquelyurbanconditions,ontheestablishmentandsurvivalofM.tenebricosa.Scalesinthewarmer
chambersdevelopedfaster,reachedhigherdensities,andhadgreatersurvival[58].Theseresults
indicatethatthebenefitsofwarmingonearlystagesettlementandsurvivalareimportantinreaching
highscaledensitiesonalreadywarmerurbantreesandmayalsobenefitscaleswhenforestswarm.
Invasivetrait:rangeexpansion.Invasivespeciesareoftencharacterizedbygeographicrange
expansionintopreviouslyunoccupiedareas[99].In1922,therangeofM.tenebricosawasdelimited
toincludestatesfromMarylandinthenorthtoFloridainsouthalongtheeastcoastoftheUSAand
westwardfromMissouritoTexas.Recentsurveyse.g.,[53,85]havefoundthemthroughoutthe
southeasternUS,inagreementwiththeMetcalf(1922)map.Wesurveyedredmaplestreettreesin
Insects2020,11,1429of16
Boston,MA,Queens,NY,Philadelphia,PA,Newark,DE,andBaltimore,MD,alongtheeastcoastof
theUS.Eachofthesecitiesisnorthofthe1922M.tenebricosadistribution.ThesesurveysrevealedM.
tenebricosainQueens(1of40trees),Philadelphia(4of7trees),Newark(18of35trees),andin
Baltimore(6of33trees)[57,60].NoM.tenebricosawerefoundinBoston(39trees).Inaddition,we
surveyedredmaplesinAsheville,NC(elevation:650m)andfoundM.tenebricosaon12of35trees
[61]inacountynotpreviouslyrecordedashavingM.tenebricosa[83].ThesefindingssuggestM.
tenebricosacanexistatlatitudesnorthorelevationsgreaterthanitspreviousdistributionlikelydue
tocombinedeffectsoftheUHIeffectandclimatewarmingthatreducewintertemperatureextremes
andreducesthefrequencyoflethalcoldevents[100].Theseobservationscouldbefollowedupwith
researchtoidentifythemechanisms(e.g.,thermaltolerance[101])relatedtothisrangemovementin
citiesandwhetherM.tenebricosahasspreadtoruralornaturalforestsinthelastcentury.
3.CitiesSimulateClimateChange
Thereisevidencethatcitiescanhavesimilareffectsonplantandanimalspeciesasthose
predictedbyoutdoorwarmingexperimentsandexperimentsingrowthchambers[29].Thewaxy
testsofM.tenebricosaremainonplantsaftertheinsectsdieand,thus,arepreservedonherbarium
specimens.Youngsteadtetal.(2014)inspected342redmapleherbariumspecimenscollectedin
forestsfrom1895to2011fromNorthCarolina,SouthCarolina,andGeorgia.Melanaspistenebricosa
werecountedoneachspecimenandtemperaturewasestimatedforthecollectionlocationbyyearof
collection.Theyalsocollectedtwigsandtemperaturesfromurbanredmaples.Themodeledresponse
ofherbariumandurbanscaletotemperaturewassimilarinshapebutdifferentinmagnitudewith
urbanscalesfoundatsixtimesgreaterdensity.Melanaspistenebricosawasfoundonapproximately
29%ofsitesfromherbariumspecimens.ThefrequencyofM.tenebricosaonsampleswasgreatestin
historicallywarmperiodsofthe20thcenturyandlowerinhistoricallycoolperiods.Thisdocuments
fluctuationinscaleoccurrencewithclimateinforestsandthepotentialforextendedwarmingto
makeM.tenebricosamorecommoninforests.Warminginthepast40yearshasbeengreaterin
magnitudeanddurationthantheotherwarmperiodsanalyzedinitially.Todeterminehowrecent
extendedwarmingaffectedM.tenebricosadensity,20forestsiteswhereherbariumspecimenshad
beencollectedwererevisited.Randomtwigswerecollectedfromredmaplesateachsiteand
processedforstoragethatmatchedtheproceduresoftheherbariumsamples.At16ofthesites,scale
densityhadincreasedcomparedtotwothatwerethesameandtwothatdeclined[87].WithintheM.
tenebricosanativerange,warmingincreasesscaleoccurrenceanddensityinforestswherethey
generallyoccuratlowdensities,thusprovidingevidenceforpotentialfuturespreadintoforests.
Moreover,recentreviewshaveevaluatedthepotentialforandevidenceofrangeexpansionforplant
pestsandpathogenswithwarming[102,103].
4.Conclusions
Mostherbivorousarthropodsarenotpests.Theyarebackgroundherbivoresthatcontributeto
thebiodiversityandfunctioningofecosystems.Yet,nativeandexoticsleeperspeciesareagrowing
threattoforestsandotherecosystemswithcontinuedwarming.Here,weillustratedhowcities
provideauniqueopportunitytostudythecomplexeffectsofwarmingoninsectherbivores.Thetwo
scaleinsectspeciespresentedshowmultipleinvasivetraitsonurbantreesduetotheUHIeffect.The
effectsofwarmingwerealsodetectedinlaboratoryexperimentsandforestobservationssupporting
theassertionthatwarmingisdrivingthescaledensityandthephenotypicchangesobservedrather
thanotherurbanfactors.Manyotherscalespeciesarechronicoroccasionalpestsonurbantreesand
temperatureisunlikelytobetheprimarydriverofeveryspecies.Geographicallynativespeciessuch
astuliptreescale,obscurescale,pineneedlescale,andothersintheUSareimportantpestsofurban
treesthoughmechanismsthatdrivethesepestsarenotwellestablished[19,49,104].Treestress,
depauperatenaturalenemycommunities,insecticides,andfertilizerhaveallbeenattributedtohigh
densitiesofscaleinsectsandotherpestsonurbantrees[18,19,94,105,106].Connectionsbetween
temperatureandscaleoutbreakshavebeendescribedrelativelyrecentlybutmayhelpunifysome
Insects2020,11,14210of16
otherproposedmechanismssince,forexample,heatiscausedbyimpervioussurfacesthatalso
fragmentandreducenaturalenemyhabitatsandcausetreestress[20].
Scalesandtheirrelativescankillorsickentreesacrossvastgeographicareas[107,108],changing
thestructureandfunctionsofforestecosystems[109–111].Warmingcanbenefitmanyofthesepests
directlyandindirectlyincreasingsurvival,reproduction,andpopulationgrowth[112].Higherfitness
forpestscombinedwithpotentiallygreaterstressoftheirhosttreesisexpectedtoincreasethespread
andpestilenceofgeographicallynativeandexoticspecies.Forexample,hemlockwoollyadelgids,
elongatehemlockscale,andthescalesassociatedwithbeechbarkdiseasebenefitfromwarmer
wintersathighlatitudeswheretheywouldotherwisenotsurvive[113–116].Thegeographicranges
ofmanyotherscaleandnonscaletreepestsarerestrictedbycoldtemperatures.Thesespecieswould
beexpectedtosurviveoreventhriveincitiesatlatitudeshigherthanwheretheyoccurinforests.
ThisiswhatweseeingloomyscalebutalsopineprocessionarymothwhichsurvivesintheParis,FR
heatislandalthoughitisnorthofthenaturalexpansionfront[117].TheUHIeffectbenefitspine
processionarymothcaterpillarsbyincreasingdevelopmentrateandwintersurvival[118].
Notallarthropodsbenefitfromhighertemperatures.NegativeeffectsoftheUHIeffecthave
beendocumentedformanynonpestarthropodspecies,includingsomeants,bees,butterflies,and
spiders[24,27,28,119].However,negativeeffectsofwarminghavealsobeendocumentedforsome
pestspecies,includingAdelgestsugae(Annand)(hemlockwoolyadelgid)[120],LymantriadisparL.
(gypsymoth)[121],Matsucoccusmatsumurae(Kuwana)(pinebestscale)[122],andM.tenebricosa[101]
wherestudiesoneachhaveshownevidenceforrangestasisorcontractionwithwarming.Thus,the
UHIeffectcannotonlyportendtheawakeningofpestspeciesthatbenefitfromwarmingbutalso
identifyspeciesdestinetodeclinewithclimatewarming.Identifyingandstudyingpestilenturban
speciescouldbeapragmaticapproachforidentifyingandpreparingforsleeperspecies[29].
Furtherresearchisneededtodeterminewhetherthisapproachappliesbroadlytoarthropods,
otherectotherms,plants,andevenpathogens.Researchinsomeofthesesystemshasidentified
speciesthatareconsideredlatentinvasiveorpestspecies(e.g.,insects[123],pathogens[124]),where
theyremainquiescentuntilconditionsaremoresuitable.Apragmaticstartingpointforresearchto
identifyotherpotentialsleeperspecieswouldbetoexaminethoseinsectsthatarealreadypestsor
moreabundantincities.Forexample,Thyridopteryxephemeraeformis(Haworth)(bagworms)arean
urbantreepestwhosedistributionislimitedbycoldtemperatures[125,126],buthavedemonstrated
greatersurvivalinareaswithgreaterimpervioussurface[127].InEurope,Eotetranychustiliarum
Hermann(limemite)hadfourtimesgreaterabundanceandthreetimesgreaterfecundityonTiliasp.
(linden)treesthatwereonthesunniersideofthestreetascomparedtomitesontreesontheshadier
side[128].TheoverwinteringsurvivalofHornadaulaanisocentraMeyrick(mimosawebworm)was
greaterontreesorbranchesthatwerenearerbuildingsandmoreprotectedfromthecold[23].Given
thebenefitsoftheUHIeffectonthesespecies,theirpotentialtobefutureforestpestsmaybesimilar
tothescaleswediscusshere.However,importantly,futuremonitoringwilldocumentwhether
gloomyscale,oaklecaniumscale,andotherpotentialsleeperspeciesactuallybecomeforestpestsas
predicted.
AuthorContributions:Conceptualization,S.D.F.andM.G.J.;WritingOriginalDraftPreparation,S.D.F.and
M.G.J.;WritingReview&Editing,S.D.F.andM.G.J.;FundingAcquisition,S.D.F.andM.G.J.Allauthorshave
readandagreedtothepublishedversionofthemanuscript.
Funding:ThisworkissupportedbyaPostdoctoralFellowship(grantno.20196701229633)fromtheU.S.
DepartmentofAgriculture,NationalInstituteofFoodandAgriculturetoMGJaswellasUSDANIFAaward
numbers20167000625827and20187000628914toSDF.Theprojectdescribedinthispublicationwasalso
supportedbyCooperativeAgreementsG15AP00153andG19AP00041fromtheUnitedStatesGeologicalSurvey
toSDF.Itscontentsaresolelytheresponsibilityoftheauthorsanddonotnecessarilyrepresenttheviewsofthe
SoutheastClimateAdaptionScienceCenterortheUSGS.
ConflictsofInterest:Theauthorsdeclarenoconflictsofinterest.
Insects2020,11,14211of16
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