REVISTA
BRASILEIRA
DE
Entomologia
AJournalonInsectDiversityandEvolutionw w w . r b e n t o m o l o g i a . c o m
Biological
Control
and
Crop
Protection
Uncovering
the
spatial
pattern
of
invasion
of
the
honeybee
pest
small
hive
beetle,
Aethina
tumida,
in
Italy
Alessandro
Cini
a,∗,
Ugo
Santosuosso
b,
Alessio
Papini
aaUniversitàdegliStudidiFirenze,DipartimentodiBiologia,viaMadonnadelPiano6,Florence,Italy
bUniversitàdegliStudidiFirenze,DipartimentodiMedicinaclinicaesperimentale,LargoBrambilla3,Florence,Italy
a
r
t
i
c
l
e
i
n
f
o
Articlehistory:
Received19September2018
Accepted27November2018
Availableonlinexxx
AssociateEditor:EduardoAlmeida
Keywords:
Apismellifera
DBSCAN
Invasivealienspecies
Pestspecies
Spatialdynamics
Smallhivebeetle
Notifiabledisease
a
b
s
t
r
a
c
t
Thefasttrackingofinvasionspatialpatternsofalienspeciesiscrucialfortheimplementationof pre-ventiveandmanagementstrategiesofthosespecies.Recently,ahoneybeepest,thesmallhivebeetle Aethinatumida(hereafterSHB),hasbeenreportedinItaly,whereitcolonizedmorethan50apiariesinan areaofabout300km2.SHBisanestparasiteandscavengerofhoneybeecoloniesnativeofSub-Saharian
Africa.Likelybeinghelpedbytheglobalizationofapiculture,SHBunderwentseveralinvasionsinthelast twentyyears,causinglocallyrelevanteconomicimpact.Whilemanyfeaturesofitsbiologyhavebeen addressed,animportantknowledgegapconcernsthespatialinvasiondynamicsininvadedareas.Inthis paperwecoupledtwospatialanalysistechniques(geographicprofilingandadensity-basedspatial clus-teringalgorithm)touncoverthepossibleinvasionpatternofSHBinItaly.Weidentifiedtheporttown ofGioiaTauroasthemostlikelypointfromwhichSHBmayhavespreadandsuggestedthepossible successiveaxesofdiffusion.TheseputativediffusionpathssuggestthattheSHBspreadinsouthItaly mighthavebeenduetoamixofnaturaldispersalbetweencloseapiariesandlongerdistancemovement throughfaster,likelyhuman-mediated,communicationroutes.
©2018PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeEntomologia.Thisisan openaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/
).
Introduction
ThefasttrackingofthespatialpatternofInvasiveAlienSpecies (hereafterIAS) invasion innewareas rightaftertheirarrival is ofoverwhelmingimportanceinordertoadoptfruitfulpreventive strategiestoreducethespreadofIASintheinvadedareas, pre-vent possiblerecurrentintroductions and preparemanagement protocols(Hulmeetal.,2008).Aneffectiveandfastreactiontothe invasionisfacilitatedbytheidentificationofthepossiblespreading centre(s)andtheearlypost-invasiondiffusionpathways.
SHBisasub-Sahariancoleopteran,exotictoEurope,whichhas beendetectedinSouthItalysinceabout5years(Mutinellietal.,
2014;Palmerietal.,2015).Morerecently,newinvasionsofthis
pestwererecorded inBrazilwhere itappears tobestillatthe beginningofitsspread(Toufailiaetal.,2017).SHBisaparasiteand scavengerofhoneybeecolonies,andbothSHBlarvaeandadults feedonhoney,pollen,beelarvaeandalsoondeadadultbees(Ellis
etal.,2002;Neumannetal.,2016).Themainimpactonhoneybee
isrelatedtolarvaefeedingoncombs,whichsometimesmayresult
∗ Correspondingauthor.
E-mail:cini.ales@gmail.com(A.Cini).
ina complete collapseofthenest (Schmolke,1974).Additional damagesmayalsobeprovokedbySHBattackingstockedhoneybee products,suchascombsinstoragecontaininghoney(Elzenetal., 1999)and,potentially,spreadingofbeeviruses(Eyeretal.,2009). WhileSHBdoesnotrepresentarelevantpestspeciesinitsnative range,itcancausefrommoderatetobigimpactsininvadedareas
(NeumannandElzen,2004;Spiewoketal.,2007).Finally,SHBhas
beensuggestedtobeabletoexploitcoloniesofotherApidae,such asbumblebeesandstinglessbees(SpiewokandNeumann,2006;
Hoffmannetal.,2008).
SHBmovedrepeatedlyacrossinternationalborders,leadingto aworldwidediasporathatbroughtittocolonizeseveralstatesin theU.S.,Australia,Korea,SouthAmericaandalsoinvadingCanada, evenifinthelattercountryfastdetection,movementrestrictions andpossiblyalsoclimaticconditionsallowedtoavoid
establish-ment(Lounsberryetal.,2010;AlToufailiaetal.,2017;Leeetal.,
2017).
Europe (where SHB is a honeybeenotifiable pest, Commis-sionDecision2004/216/EC)faced theriskofaninvasionforthe firstdocumentedtimein2004,whenSHBwasdetectedin Portu-galduringqueenbeeimportcontrolinthelaboratory(Murilhas, 2004)andrapidlydestroyed.In September2014SHBwasagain reportedinEurope,havingbeenspottedinthreehoneybeenucleus
https://doi.org/10.1016/j.rbe.2018.11.005
0085-5626/©2018PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeEntomologia.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://
coloniesin SouthItaly, nearthecoastlineof regionofCalabria, whereithasprobablyaccidentallyintroducedfromAfrica(Granato et al.,2017).SHB wasdetectedin 58 apiaries and one natural colony,spanningoveranareaofabout316km2 (Mutinellietal.,
2014).Newinfestedapiarieshavebeendetectedin2015,2016and
2017(http://www.izsvenezie.com/aethina-tumida-in-italy/), and
theinvasionisthusnotresolved.
Despiteresearcheffortsstronglyincreasedtheknowledgeon SHBduringthelastfewyears,manyknowledgegapsstillremain (Neumanetal.,2016).Amongthem,oneofthetopprioritiesisto understandtheinvasiondynamics,inparticularlythespatial pat-ternofdiffusionafterthearrivalinnewareas(NeumannandElzen,
2004).
Here,weproposeatwo-stepspatialanalysisinorderto iden-tifythepossiblepost-invasionspatialdynamicsofIASstartingfrom presence-onlyreports,usingtherecentinvasionofsmallhive bee-tleAethinatumidaMurray,1867(Coleoptera:Nitidulidae,hereafter SHB)asamodel.Thedetectionofspreadingcentres,inadditionto facilitatethepreventionofrecurrentIASintroduction,mayalso allowtheidentificationofthepossibleidiosyncraticfeaturesthat boostedtheinvasion(e.g.ecologicalrequirements).Startingfrom thespreadingcentre(s),diffusionmaythentakeplaceinseveral spatialways,beinginfluencedbytheecologicalneedsandlife his-torytraitsoftheIASaswellastheenvironmentalheterogeneityand possibleman-assisteddisplacement(Wilsonetal.,2009).Our anal-ysisaimsto(a)identifythemostlikelyspreadingcentre,(b)infer thelikelyearlypost-invasiondiffusionpathwaysofSHBinvasion inItalyand(c)provideamodelforotherinvasionsofA.tumidain othergeographicalareas.IASspreadingcentre(s)arethoseinvaded areas which more likely allowed the first successful establish-mentoftheIASandthankstowhichtheIASthenspreadtoother areas.
InordertoinferthepossibleinvasiondynamicsofSHBinItaly frompresencereports, wecoupledGeographicprofiling– here-afterGP–(Rossmo,2000),amodellingtechniquewidelyusedto inferspreadingcentreofinvasivespecies,togetherwitha density-basedspatial clustering algorithm (DBSCAN, Esteret al., 1996). Geographicprofiling(GP)isananalytictoolfortheidentification ofthegeometricaloriginoflinkedevents,whichhasbeenrecently appliedtoarangeofecologicalissues,amongwhichthe identifica-tionofthesourcepopulation(s)ofinvasivespeciesusingtheknown positionsoftheircurrentpopulations(Stevensonetal.,2012;Cini
etal.,2014;Faulkneretal.,2017;Papinietal.,2013,2017a,b),while
severalenhancementsofthemethodareunderstudyinorderto refinethereliabilityoftheanalysis(PapiniandSantosuosso,2017;
SantosuossoandPapini,2018).
TheDBSCANisaclusteringalgorithmdefinedasdensitybasedas itproducesclustersofpoints(onaplane)thataregroupedtogether accordingtotheconceptthateachpointoftheclustermustbeclose toatleastagivennumberpofotherpointsoftheclusterswithina givenradiusr(XuandWunsch,2005).DBSCANhasseveralfeatures thatseemadvantageousinbiological invasions,since itisquite robusttooutliers(Smithetal.,2002),minimallyaffectedbypoints orderinganditrequireslittleaprioriinformationaboutthedataset parametersvalues,suchasnumberandshapeoftheclusters(Smiti
andEloudi,2013),acasewhichistypicalofbiologicalinvasionsin
theirfirstyearsafterIASintroduction.
OuraimwastodrawthelikelyspatialpatternofSHBinvasionin Italy,thussettingthestageforfurtherimplementationofspecific monitoringprotocolsinthisarea.
Materialandmethods Datacollection
SHB presence data were retrieved from Mutinelli et al.
(2014)which providesthedata oftheNational Reference
Cen-treforApiculture(availableat
http://www.izsvenezie.it/aethina-tumida-in-italia/), collected during theapiary surveillance
pro-grammeafterthediscoveryofSHBinItaly.Briefly,asubsample oftheapiarypresentinaradiusof20and100kmfromthefirst reportwereinspected,andapiarywereconsideredinfestedifat leastonehiveshowedthepresenceofSHB,inanydevelopmental stage.Asgeoreferentiationofinfestedapiariesisnotfreely avail-ableduetoprivacyreasons,wegeoreferencedapiarysitedirectly fromthemap.Usingthisprocedureestimatedspatialaccuracywas 25metres,whichwasthusnotexpectedtoaffecttheresolution atwhichourspatialanalysiswasperformed(tenstohundredsof kilometres).Aswefocusontheveryearlypost-invasiondynamics inthearrivalzone(Calabriaregion)andweaimedat understand-ingpossibleaxesofdiffusionusingonlyearlypost-invasionsdata, wedidnottakeintoaccountthepresencereportfromSicily(one infected colonies in a 56-hives migratory apiary, likely due to humanhivetranslocation, Mutinelliet al.,2014), northe pres-encedatareferringto2015or2016surveys,anapproachalready used(Cinietal.,2014).Moreover,2015and2016datahavebeen collectedaftersanitarymeasures,suchashivedestruction,were performed,sothattheymightnotproperlyrepresenttheinitial spatialdynamicsofSHB.DataweremappedontheSouthItalymap (obtainedbytheopenaccesswebsitewww.openstreetmap.org). Identificationofthemostlikelyspreadingcentre:geographic profiling
GPusescoordinatesonamapoflinkedevents(e.g.locations whereanIAShasbeenreported)togenerateaprobabilitysurface, whichwillbesuperimposedontheoriginalmaptoproducethe so-calledgeoprofile.Suchgeoprofiles,basedonlyonpresencedata,do notprovidetheexactoriginoftheevents,butproducesdecreasing probabilitydensity,thusprioritizinggeographicalareas(Rossmo, 2000)wheremonitoringprotocolsshouldbeimplementedand tar-getedresearchescarriedout.WeusedthemodelforGeoprofiling analysisdescribedbyRossmo(2000)andmodified accordingto
Papinietal.(2013).Foreachpixelwithcoordinates(i,j)ofthe
tar-getarea,thescorefunction(p)iscalculatedasfollows(redrawn
fromStevensonetal.,2012):
Pij=k∗ c
n=1⎡
⎢
⎣
(xi−xn)2+(yi−yn)2 f + (1−)∗B (f−g) 2B− (xi−xn)2+(yi−yn)2 g⎤
⎥
⎦
where: = 1, ifdistance > B 0, otherwiseForapointPofcoordinates(i,j)theformulasumsthe prob-abilityacrossallthelocationswheretheinvadingorganismwas found.Thismodelisbasedontwocomponents:adistancedecay function(inwhichtheprobabilityofapresencereportdecreases asdistance fromtheinvasion site increases)and a bufferzone ofradiusB,withinwhichthelikelihoodincreaseswhendistance
Fig.1. GraphicalexplanationoftheDBscanalgorithm.Itemswithinagivendistance
(radius)r(indicatedascircles)fromatleastagivennumberp(threeintheexample)
ofotherpointsareassignedtothesamecluster(i.e.thebluecirclesallbelongtothe
sameclusterbecauseeachbluecircleiswithinagivenradiusrofthreeotherblue
circles).Thetwogreenitemscannotbeassignedtothebluecluster,sincetheyare
withindistancerfromfewerthanthreepointsofthebluecluster.Thereditemis
positionedatadistancethatis≥todistanceAandthereforeitdoesnotbelongto
thebluecluster.
increases.Thedistance-decayfunctioncanbeexplainedby disper-salcostswhilethebufferzonemaybeduetohabitatunsuitabilityof invasionsites.Stevensonetal.(2012)suggestedthatitis conceiv-abletousegeneral,taxonorhabitatspecificvaluesforthemodel parametersincaseswherenodataonthetargetspeciesexist.In ourcase,wechosemodelparametersaccordingtopreviously pub-lishedanalysesoninvertebrateinvasivespecies,suchasStevenson
etal.(2012)andCinietal.(2014).Sincewedonothaveany
infor-mationaboutthepossiblerealvaluesofthecrucialbufferzone radius(B)forthis orrelatedspecies,and sinceitmightdepend onseveralfactors(suchasdispersal ability,habitat heterogene-ity,etc.),weselectedthevaluesobtainedfortheonlyavailable insectspeciesfromStevensonetal.(2012)(Bvalues:0.38–0.42), which,scaledtoourmapwasaboutB=10(itisnot straightfor-wardtoobtainthisdata,sinceStevensonet al.didnotindicate howlargeisBinkmortheresolutionoftheirmap).Inorderto evaluatetherobustnessofthemodelwhenBvaries,weranthe analysisusingBvaluesrangingfromB=5toB=20 (correspond-ingtoa rangeof about0.125–5km),which spanned acrossthe valuesfoundforotherterrestrialflyinginsects(Stevensonetal., 2012,adaptedtothedifferentmapscale).Forthispurposeweused thepythonscriptwrittenbytheauthors:Geoprof205csv.pyon Bitbucket(https://bitbucket.org/ugosnt/alandugo/).
Identificationofthepossiblediffusionpathways:clusteranalysis anddensitymaps
TheDBSCANalgorithmwasusedtoproduceclustersofpoints correspondingto observations on theused map. The points of a given cluster must beclose to at least a given number p of other points within a given radius r (Xu and Wunsch, 2005) (Fig.1).Inordertoseparatedifferentclustersofobservationswe usedthefollowingalgorithmsimplemented inpython: Kmeans (number of clusters assessed with Silhouette) (Python script Kmeanssil002.py)withthefollowingspaceVoronoitessellation asproposedindetailbySantosuosso andPapini(2016)andthe Density-basedspatialclustering(DBSCAN),asdefinedbyEsteretal.
(1996). DBSCANwas implementedin Python as dbscan1.0.0.py
andafterpreliminarytrialsweusedr=6(pixels),corresponding toabout100mand p=5 (numberofpoints tobefoundwithin theradius)asparameters.Finally,inordertoinferpossiblespatial invasiondynamics,wecoupledGPandDBSCANresultsbydrawing theputativeinvasiondirectionsconsideringasastartingpointthe
centreoftheidentified95%spreadingareasidentifiedbytheGP andthetipofeachdirectionarrowsasthecentreofmassofeach clusteridentifiedbyDBSCANmethod.
Results
TheGPanalysisidentifiedanareaofabout27km2onthecoast,
north/northeast ofthe townof GioiaTauroas the95%(in red) mostlikelyspreadingcentreofSHBinSouthItaly(Fig.2a)onthe basisoftheinfectedapiaries.Overlappingtheareaidentifiedby GPasthespreadingcentre,usingasinputsourcesinfectedapiary onlyorbothinfectedandnoninfectedapiary(nullmodel,Fig.2b), showedthatthesecondareaof95%probability(inred)oforigin, waslocatedinamorenorthernpositionwithrespecttothefirst (onlyinfectedapiaries),suggestingthattheareaidentifiedbyGP wasnotsimplyreflectingapiarydensity.Theintersectionbetween thetwoareasisshowninFig.2canditcorrespondstolessthan 4%ofthetotalnumberofredpixels,whichcanbeconsidereda significantdifference.GPresultsarerobust,asvaryingtheBvalue, theresultaboutthelocalizationoftheareaofhighestprobability ofspreadingcentredidnotvarymorethanfewpixels(datanot shown).
DBSCANclusterizationassigned the57 casesofinfected api-aries tothree clustersand identified17 apiariesasoutliers(i.e. notnecessarilybelongingtoanycluster).Twoofthethree clus-tersfallindeedattheborderofthespreadingcentreidentifiedby theGPapproach(compareFig.2withFig.3).Thethirdone(as pur-pleovalsinFig.3)isabout10kmsouthwardfromGioiaTauroand about15fromtheputativespreadingcentre,asidentifiedbyGP. Consideringthiscoupledanalysis,itseemsverylikelythatamain axisofSHBspread,pointingsouthward,canbeidentified(Fig.3a andb).
Discussion
Theidentifiedareaofabout27km2 aroundthePortofGioia
TauroasthemostlikelyspreadingcentreofSHBinItalysupports thestrictrelationshipofthisinvasionwiththepresenceofoneof themostimportantportsinSouthItaly.
Theposition ofthethree main clustersof SHB identifiedby the DBSCAN analysis showed that while two are close to the supposed spreading centre (tentatively identifiedwith GP), the thirdoneispositioned15kmsouthward.Thiscoupledapproach thussuggests(a)thataport,GioiaTauro,mightbetheentrance, and (b) that SHB might have had three main diffusion direc-tions,withdifferenteasinessofpenetrationalongdifferentspatial gradients.
Theimportanceofmarineportsaslikely pointsofIASentry hasbeenwidelyrecognized(Kelleretal.,2011;McCulloughetal., 2006).Travelers’baggage,cargoandtradeitemsmayeasily intro-duceexoticinvertebratesandplantweedsfromallovertheworld. Severalalieninsectsareindeedsuspectedofhavingspreadinto newareasdiffusingfrommarineporttown.Itisthecaseof wood-boringbeetles(Haack,2001)andofthesmallfruitpestDrosophila suzukii(Cinietal.,2014).Indeed,thepossibilitythatSHBmight alsoenterthroughportshasbeenproposedfortheUSAEast-coast andAustraliainvasions(Hood,2004)andwasalreadysuggested forItaly(Mutinellietal.,2014).OurGPapproachstronglysupports thissuggestion.
Thefindingof twovery closeclustersand onemoredistant southern cluster suggeststhat SHB Italian invasion might have proceededthankstoamixofleading-edgedispersal(i.e.diffusive spread from the edge of the invasion range, likely driven by naturaldispersal)andjumpdispersal(long-distancedispersalover substantial distances likely due to accidental human mediated
Fig.2.Identificationofthepossiblediffusioncentre.(a)The95%mostlikelyspreadingcentreisinredandcorrespondstotheresultsofthegeographicprofiling(GP)applied
onlytotheinfectedapiaries;(b)anullmodel,withGPresults(theredareas)basedonalltheapiariespresentinthearea,bothinfectedanduninfected.Theredareais
localizedinamorenorthernareawithrespectto(a);(c)intersectionoftheredareas(a)and(b).Sincetheintersectionislessthan5%(inourcasethedifferenceis4%orless)
ofthetotalredarea,wecanconsiderthedifferenceassignificant.Thebluepointscorrespondtouninfectedapiariesandredpointstoinfectedapiaries.(c)ispositionedin
themiddlebetween(a)and(b)tobettershowtheintersection.×300,000.
Fig.3. PossiblespreadingpathwaysfromtheidentifiedspreadingcentrearemappedintheinvadedregiononthebasisofthealgorithmDBSCAN.Thepinkandbluelines
representtheVoronoitessellationofthespaceaftertheKmeansanalysisforthreeclusters(checkedwithSilhouettemethod,seethetext).Thedashedarrowsconnectthe
centroidoftheclustersandshouldgivesuggestionsabouttheaxesofdiffusion.(a)ResultsoftheGPanalysis.(b)Representationoftherecordedobservations(infection
cases)ontheterritorywiththerepresentativesofthedifferentclustershighlightedwithdifferentcolours.Thebluepointscorrespondtouninfectedapiaries.×250,000.
transport), in agreement with previous findings (Hood, 2004;
Spiewoketal.,2008).WemustalsoconsiderthatwindsinCalabria
blowmostcommonlynorthwardfromsouthandsoutheastregions
(FratianniandAcquaotta,2017),andthethirdmostdistantcluster
ispositionedjustsouthtothefirsttwo.Hence,dispersalappears tobeintheoppositedirectionwithrespecttothesiroccowind. Moreover,intheareaofthethirdclusternomainroadispresent, henceapparentlythespreadingwasdue toshortdistancelocal movements.Theproposalofaspreadingmodelwithbeekeepers infesting their other apiaries through ‘unintentional transfer’ was called “distance and ownership model” (EFSA, 2015) and thismodelofspreadingwouldbesupportedbyourdata.Onthe contrarythe first two northern clustersare in industrial areas wherethehumanpresenceisverycommon:herethespreading occurredatrelativelylowdistance(lessthan1km)and maybe
due partly to thenatural movement of the pest and partly by accidentaltransportbyhumanactivity.
Policiestoreducetheriskoffurtherspreadingofthepestmaybe hencecentredmainlyontheregulationoftheactivityofbeekeepers proposingguidelinesaimingtoreducethetransferofmaterialfrom onehivetoanotherortotransporthivesfromoneareatoanother. Aswithanymodellingapproach,GPhassomelimitations.First, itsreliabilityreflectstheaccuracyofpresencedata.Unfortunately, standardizedpresencedataareverydifficulttoobtainforinvasive speciesrightaftertheirinvasion.IntheSHBcasepresentedhere, contrarytowhatusuallyhappenswithmanyIAS,thepestspecies wasalreadyrecognizedasahoneybeenotifiablepest (Commis-sionDecision2004/216/EC),sothatveterinaryservicesrapidlyput inplaceastandardizedsurveyinawideareaaroundthefirstSHB reports(Mutinellietal.,2014),whichresultedinareliabledatabase,
thusprovidingstrengthtoourmodellingapproach.Asecond pos-siblesourceofbiasedsamplingisrepresentedbytheabilityofSHB tosurviveonnon-honeybeerelatedresources,suchasrottenand fermentingfruitsorotherspecies(suchasbumblebees,Hoffmann etal.,2008),whichmightrepresentarefugeforSHBallowing fur-therre-infestations(NeumannandElzen,2004).However,sofar noSHBhasbeendetectedonrottenfruitsinafieldinvestigation carriedoutintheinfestedareabetween2014and2015suggesting thatfermentingfruitsdonotrepresentapossiblealternativefood resourceforSHBinCalabria(Mutinellietal.,2015).However,ithas beenshownthatthesealternativeresourcesarelesspreferredand lesssuccessfulfoodsources,thatalsoreduceSHBfitness(Ellisetal., 2002),sothatweareconfidentthattheuseddatasetrepresenta reliablepresencedataset.
Despite these possiblelimitations, we thus believethat our resultsprovideafirstreliablehypothesisofSHBinvasiondynamics inItaly,supportingthehypothesisofaseaportmediatedinvasion
(Mutinellietal.,2014forItaly,andHood,2004forUSandAustralia),
andfurtherhighlightingtheroleofseaportsasIASintroduction sites(Macketal.,2000).TheVoronoitessellationandthedashed lineslinkinggroupsofobservations(seeFig.3a)shouldrepresent anestimateofthespreadingdirection,whilethedistancefromthe hypothesizedpointoforigin,relatedtotheguessedtimeofarrival ofSHB,shouldgiveanideaaboutthespeedofthediffusionitself intheterritory.
Moregenerally,webelieveourresultsshowthatthecouplingof GPandDBSCANmightrepresentapromisingandrapidapproach tousethesedatatoprioritizeareas,insideIASinvadedranges,in whichtofocusfuturemonitoringandmanagingefforts.
Thisanalysismaybeusedefficientlyinareaswheretheinvasion isstillatthebeginningasinBrazil(AlToufailiaetal.,2017),inorder tobetterunderstandthecausesoftheinvasionanditsspreading directionsinordertoundertakesuitableactions.
Compliancewithethicalstandards
Thisarticledoesnotcontainanystudieswithhumanorother animalparticipantsperformedbyanyoftheauthors.
Authorcontributionstatement
AC,USandAPconceivedresearch.ACcollectedthedata.AC,US andAPanalyzedthedata.ACwrotethemanuscript.Allauthors readandapprovedthemanuscript.
Conflictofinterest
Theauthorsdeclarenoconflictsofinterest. References
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