the march of the common green iguana (iguana iguana ... · the common green iguana (iguana iguana,...

1

ThemarchoftheCommonGreenIguana(Iguanaiguana):earlyestablishmentin

SingaporeandThailandisfacilitatedbythepettradeandrecreationalparks

MatthijsP.vandenBurg1*,StevenM.VanBelleghem2,ChristinaN.DeJesúsVillanueva3,4

1DepartmentofBiogeographyandGlobalChange,MuseoNacionaldeCienciasNaturales,SpanishNationalResearchCouncil,Madrid,Spain2DepartmentofBiology,UniversityofPuertoRico,RíoPiedras,SanJuan,PuertoRico3CollegeofEnvironmentalandLifeScience,UniversityofRhodeIsland,Kingston,RhodeIsland,USA4InternationalInstituteofTropicalForestry,UnitedStatesForestService,UnitedStatesDepartmentofAgriculture,SanJuan,PuertoRico*Correspondingauthor.email:thijs.burg@gmail.com.

Abstract

ThepopularityoftheCommonGreenIguana(Iguanaiguana)asapethascontributedto

itsglobaloccurrenceasaninvasivealienspecies.Earlydetectionandcontrolofinvasive

alienI.iguanapopulationsisnecessarytopreventtheneedforlargeandfinancially

demandingeradicationactions.Here,wecollatedinformationfromdigitalfootageand

interviewsregardingsightingsoffreeroamingI.iguanaspecimensinSingaporeand

Thailand,andpresentevidenceofearly-stageinvasionsandestablishment.Using

speciesdistributionmodeling,wefindthatlargepartsofThailandandneighboring

countrieshavesuitablehabitat,whichcouldfacilitatetheexpansionofthesealien

populationsifleftuncontrolled.Additionally,wereportsingularI.iguanasightingsin

HongKongandPeninsularMalaysia.WecallforawarenessofalienI.iguanainthe

PhilippinesduetothehighnumberofpetiguanasandreportedCITESimportationsas

wellastheavailabilityofsuitablehabitatthroughoutthearchipelago.Further,we

identifyI.iguanapresencetobefacilitatedbythereleaseofpet-tradedspecimensand

uncontrolledexhibitionpracticesinrecreationalparks.Weproviderecommendations

forimplementingmonitoringanderadicationeffortsandstrategyrecommendationsto

haltfuturespreadandrelease.

Keywords:CITES,Citizenscience,Invasivealienspecies,Legislation,Rangeexpansion,

Socialmedia,Wildlifetrade

Introduction

TheCommonGreenIguana(Iguanaiguana,Linnaeus,1758)isaheavilytradedreptilian

petspeciesthathasseenitsglobaltransportregulatedsince1977(CITES2019).Despite

regulation,thepettradeisanimportantcontributortotheoriginofinvasive

2

populations(Falcónetal.2013;Bocketal.2018;DeJesúsVillanuevaetal.under

review),althoughotherintroductionfacilitatorsareknown(Censkyetal.1998;vanden

Burgetal.2020).IguanaiguanaoccursthroughoutCentralandSouthAmericaaswellas

onseveralCaribbeanislands(Stephenetal.2013;Bocketal.2018).InvasionsofI.

iguanaaremainlyrestrictedtoCaribbeanislands,withonlyasmallsetofislandsknown

fromoutsidethisregion:CanaryIslands(Spain),Fiji,Hawaii(USA),JapanandTaiwan

(Bocketal.2018;Leeetal.2019).Importantly,establishedpopulationsofthisinvasive

alienspecies(IAS)haveneverbeensuccessfullyeradicated(Leeetal.2019;Rivera-

MilánandHaakonssoninpress).

TherapidgrowthofI.iguanapopulationscanposeathreattotheeconomyof

invadedterritories,throughinfrastructuredamageandagriculturalloss,aswellas

threatstobiodiversity(Bocketal.2018).Asinvasivepopulationscanoriginatefrom

multiplegeneticlineages(Stephenetal.2013;vandenBurgetal.2018a;DeJesús

Villanuevaetal.underreview)highgeneticdiversitymightincreaseadaptivevariation

topersevereinnon-nativeenvironments(Kolbeetal.2004).InPuertoRico,and

presumablyotherinvasiveareas,I.iguanapopulationgrowthmaybefurtheraidedbya

lownumberofpredatorsanddirectcompetitors(López-Torresetal.2011).

Furthermore,invasiveI.iguanapopulationsareathreattonativespeciesthroughdirect

competitionandhybridization(Vuillaumeetal.2015;Mossetal.2018;vandenBurget

al.2018b;vanWagensveldandvandenBurg2018).OnGrandCayman,anislandof196

km2,thepresentinvasiveI.iguanapopulationwasestimatedtoreachbetween0.9–1.9

millionindividualsinearly2018beforethestartofagovernment-financedculling

program(Rivera-MilánandHaakonssoninpress).Duringthisprogram'sinitialyear,

throughcollectiveworkof500hunters,over960,000iguanaswereremovedagainstthe

expenseof5.7millionUSD(Rivera-MilánandHaakonssoninpress).Topreventfurther

spreadofthisspeciesandtheneedformultimillion-dollareradicationprograms,rapid

managementactioniskeyduringtheinitialintroductionandestablishmentphase

(Davis2009;Blackburnetal.2011).

InsoutheastAsia,ThailandandSingaporeareconsideredimportanthubsinthe

internationalwildlifetrade(Nijman2010),withherpetofaunalsurveyreportshaving

identifiednotablediscrepanciesamongCITESimportdata,andthepresenceofseveral

non-nativespeciesinthewildinthesecountries(NijmanandShepherd2007,2010,

2011;YeoandChia2010;PooleandShepherd2016).ForThailand,Nijmanand

Shepherd(2011)foundthatover150distinctspeciesofamphibiansandreptileshad

CITESimportrecordsbetween1990–2007.Incontrast,onlytworeptiles(Trachemys

scriptaelegansandI.iguana)wererecordedinThailandduringa2011–2012inventory

3

ofwildalienvertebratefauna(Boonkuawetal.2014).ForI.iguana,Boonkuawetal.

(2014)reportedthreesightingsofsinglespecimensinThailand,allofwhichhad

disappearedbeforethereport’spublication.Singaporeismainlyregardedasanimport

andre-exportcountry(Nijmanetal.2012)andwasthemainregionalreptileimporter

between1998–2007(Nijman2010).IncontrasttoThailand,over20alienreptile

specieswerepresentinSingaporein2010(YeoandChia2010).Ofthesespecies,only

fourwereconsideredestablished(Calotesversicolor,Pareasmargaritophorus,

SiebenrockiellacrassicollisandXenochrophisvittatus);withI.iguanaknownfromonlya

fewscantrecordings(Chua2007;YeoandChia2010).However,despiteprevious

reportsoffewI.iguanaspecimens(YeoandChia2010;Boonkuawetal.2014),recent

reportsoffree-roamingI.iguanaonsocialmediaplatforms(e.g.FaceBookand

Instagram)andoniNaturalisthavesparkedourconcernoverthepotentialfor

establishedandgrowinginvasivealienpopulationstobepresentinSingaporeand

Thailand.Here,we1)summarizethecurrentextentofIguanaiguanainSingaporeand

Thailand,2)identifylocationswithsignsofearlyestablishmentanditsfacilitators,3)

predictthepotentialrangeintheabsenceoffutureeradicationaction,and4)provide

recommendationstopreventfuturereleasesandmitigatenegativeecologicaleffects.

Methods

Observations

WetracedthepresenceofalienI.iguanainSingaporeandThailandthroughverifiable

sightingsusingphotographsandvideosfromsocialmedia(FaceBookandInstagram),

Internetwebsites(www.flickr.com,www.istockphoto.com,www.shutterstock.com)and

iNaturalist.Wecontactedandinterviewedownersofonlineimageswhosecontent

suggestedthepresenceoffree-roamingI.iguanatoacquiremoredetailsincludingthe

locationwherethepicturewastaken,date,presenceoffreeroamingI.iguana,presence

ofdifferentI.iguanalifestagesandnumberofindividualspresent.Throughsnowball

sampling(whereintervieweeshadmorefootageorcontactswithsimilarfootage)we

wereabletoacquireadditionalverifiablesightingsnotpublicallyavailable.When

imagesweretakenwithinzoosorrecreationalparks(hereafterrecreationalparks)we

askedwhetherI.iguanawerekeptinholdingcagesorwerefreelyroaming.Inthelatter

case,werecordedthesefacilitiesaspotentialsourcesforcurrentandfutureinvasive

populations.

Suitablehabitatmodeling

4

TobetterunderstandthepotentialrangeofIguanaiguanainSingaporeand

Thailandaswellassurroundingcountries,weusedMaxEnt(Philipsetal.2018)as

implementedinthedismoRpackage(Hijmansetal.2017;RCoreTeam2019)tobuild

speciesdistributionmodels(SDM),forcurrentandfutureclimatescenarios.MaxEnt

usesenvironmentalandclimaticdatafromspeciesoccurrencelocalitiestobuilda

predictiveSDMofhabitatsuitability(HS)forthestudyspecies,whichrunsbetween0

(lowsuitability)and1(highsuitability).First,weacquiredI.iguanaoccurrencedata

uploadedtotheGlobalBiodiversityInformationFacility(GBIF2019)andiNaturalist.We

filtereddatarecordsbasedongeoreferenceinaccuracy(excludedwhen>50km),added

recordscollectedduringrecentfieldworkbytheauthors(forColombiaandPuertoRico)

andfromrecentpublicationsoninvasivepopulations(Kraus2019;Leeetal.2019),as

wellaslocationsinSingaporeandThailandwherehatchlingorjuvenileI.iguanahave

beenobserved.Weremovedduplicatedlocationsandobviouslyerroneousrecordsfrom

locationswithoutI.iguanabreedingpopulations(e.g.Galapagos)andwithaltitude

recordsoutsideofthespeciesrange(>1000meters;Stephenetal.2013).Remaining

recordswerethenfilteredtoretainonlyonerecordper50km2(Boriaetal.2014)to

removedistributionskewnessinlocalitydata,leavingatotalof420recordsforfinal

modelconstruction.Weretainedoccurrencedatafromestablishedalienpopulations

arguingthat,althoughinvasiveareascanholddifferentclimaticcompositionscompared

tonativeareas,localclimaticvariablesaresuitableforsuccessfulreproductionandthus

helptogeneralizeintraspecificvariationwithinI.iguana(Elithetal.2010;Briscoe

Runquistetal.2019).

TheinitialSDMmodelwasbuiltusinguncorrelatedWorldClim2.0bioclimatic

variablesandaltitudelayer(FickandHijmans2017;at2.5arc-minutesresolution).As

correlationbetweenvariablescanleadtooverfitting,weimplementedthevifstep

functionwithinthesdmpackage(NaimiandAraújo2016).Thisstepwiseprocess

identifiesthevarianceinflationfactor(VIF),ameasureofhowmuchonevariablecanbe

explainedbytheothers,foreachvariableandremovesthosewithhighVIFvalues(here

setto10;ChatterjeeandHadi2006).Afterstepwisefiltering,10variableswereretained

forthefinalmodelwitha2.0–9.1rangeofremainingVIFscores:meandiurnalrange

(BIO2),isothermality(BIO3),meantemperatureofwettestquarter(BIO8),mean

temperatureofdriestquarter(BIO9),precipitationofwettestmonth(BIO13),

precipitationofdriestmonth(BIO14),precipitationseasonality(BIO15),precipitationof

warmestquarter(BIO18),precipitationofcoldestquarter(BIO19),andaltitude.

Bioclimaticandoccurrencedatawerenextcombinedtobuildapresence-only

SDMusingMaxEnt(Philipsetal.2018)forboththecurrentandafutureclimate

5

scenario.ThesemodelsweregeneratedforsoutheastAsia,aswellasthePhilippines

giventhehighnumberofI.iguanafootageonsocialmediaplatforms.PredictionsofHS

forafutureclimatescenariowererunfor2050usingtheACmodelandrcp45for

greenhousegasemission(FickandHijmans2017).Forboththecurrentandfuture

climatescenario,asetof10SDMreplicationswererunwith80%ofrecordsusedfor

modeltrainingand20%formodeltesting.Modelperformancewasevaluatedusingthe

areaunderthecurvesummarystatistic(AUC)withone-tenthofthedata;AUCvaluesof

≥0.90indicatehighmodelperformance(Swets1988).TheHSabsencethresholdwas

determinedfromthetrainingspecificityandsensitivityasimplementedinthedismo

package(Hijmansetal.2017).

Results

ForThailand,sightinginformationwascollectedfromcontactwith15personsand

iNaturalistforrecordssince2016.Sightingsoriginatedfromatotalof12locations

distributedthroughoutThailand(Fig.1)withaminimumnumberoftotalsightingsof97

I.iguana(TableA1,SupportingInformation).Adultorsubadultlifestageswere

observedatalllocations,whereashatchlingorjuvenilelifestagesoccurredatfour

locations.Thehighestnumberofsightingsbydifferentobserverswasfoundaround

NakhonRatchasimatown(Thainame:����������)inNakhonRatchasima

province.LocationswiththehighestnumberofuniqueI.iguanawereNakhonSi

ThammarathandUbonrat,andintheUthaiThanidistrict.Lastly,atleastfour

recreationalparksexhibitnon-cagedI.iguana:ChaiNatBirdPark,ChiangMaiNight

Safari,NakhonRatchasimaZoo,andThaLatBirdPark.

ForSingapore,sightinginformationwascollectedfromiNaturalistrecords,

contactwith10persons,andfromsevenuniquegreyliteraturepublicationssince2007

(Chua2007;Yeo2014;NgandLim2015;Tay2015;Khoo2016;ChewandLow2017;

Yeo2019).Werecordedaminimumof50I.iguanasightingsfrom17locationsin

Singapore(Fig.1),ofwhichfivelocationsshowedpresenceofhatchlingsand/or

juveniles.ThehighestnumberofI.iguanasightingscomesfromtheareasurrounding

JuronghillandJurongBirdParkaswellasaroundtheWarrenGolf&CountryClub.

Recreationalparkswerenotfoundtoexhibitfree-roamingI.iguanainSingapore.

6

Fig.1LocalitieswithpresenceofIguanaiguanain(A)Thailandand(B)Singaporeshowingnumberofiguanasandyearofsighting.Colorofthemostrecentyearisdisplayedperlocation.

Besidesfree-roamingI.iguanarecordsfromSingaporeandThailand,we

recordedtwoadditionallocationsinsoutheastAsia.First,onefreeroamingadultI.

iguanawasobservedsoutheastofKualaLumpur,PeninsularMalaysia;thisanimalwas

caughtintheyardoftheobserverandwasreleasedinanareanearby.Thesecond

recordisfromtwofreeroamingadultiguanasadjacenttotheTsingTamReservoirsin

HongKong.

TheSDMsforbothcurrentandfutureclimaticconditionssuggestthepresence

ofsubstantialareawithI.iguanasuitablehabitatinThailandandsurroundingcountries

(Fig.2andFig.A1).Suitablehabitatisespeciallypresentinmainlandregionsbelow15

degreeslatitude,exceptforsomeareasinThailand,southandcentralPeninsular

Malaysiaandnon-coastalregionsinVietnam.Severalhigherlatituderegionshave

suitablehabitataswellincludingpartsoftheGulfofMartaban,andlowerelevation

areasinThailand,southernLaos,andcentralVietnam.Undera2050climatescenario

HSinonlysomeareaswillsubstantiallychangewithlessareasoflowerHSintheGulfof

Martaban,PeninsularMalaysiaandSumatra(Fig.A1,SupportingInformation).AllI.

iguanalocationsreportedherebelow14degreeslatitudeareinhighHSareas,with

thoseathigherlatitudesinareaswithmarginalorlowHS,exceptfortheUthaiThani

district(Fig.2).ForthePhilippines,thecurrentclimatemodelidentifiedsuitablehabitat

inlowlandareasonallmajorislandsandmarginalhabitatorabsenceofsuitablehabitat

forhigherelevations,especiallyonMindanao.ThemedianAUCfor10SDMreplications

7

forcurrentclimaticconditionswas0.944(50%interquartilerangesof0.942–0.946),

withamedianHSabsencethresholdof0.21;andforfutureclimateconditions(2050)

0.948(50%interquartilerangesof0.942–0.951)andmedianHSthresholdof0.28.

Fig.2SpeciesdistributionmodelsforIguanaiguanainSingapore,Thailandandsurroundingcountries.Modelsusedanabsencethresholdof0.17andhabitatsuitabilityrangesfromhigh(darkred)tolow(white).BluedotsrepresentlocationswithI.iguanapresence

8

Discussion

WereportI.iguanainvasionsandearlyestablishmentinbothSingaporeandThailand

withdetailsaboutpopulationsizeaswellasthecurrentandpotentialfuture

distribution.Inbothcountries,thepresenceofhatchlingand/orjuvenilelifestages

indicateslocalrecruitmentandongoingestablishmentofthisknowninvasivealien

species(IAS).Importantly,thisreportdescribesthesecondrecordedmainland

establishmentofI.iguana,andincreasesthenumberofknownnon-westernhemisphere

establishmentstosix;Hawaii,Fiji,Japan,Singapore,ThailandandTaiwan(Mitoand

Uesugi2004;Engemanetal.2011;Falcónetal.2013;Kraus2019;Leeetal.2019);

thoughupdatesonthestatusoftheJapaneseandHawaiianpopulationsarenecessary.

Followinginterviews,weidentifiedthelikelysourceoftheseinvasionstobepet-trade

animalsthateitherescapedorwereintentionallyreleasedbyownersorunsecurely

exhibitedinrecreationalparks.BesidesthereleaseofpetI.iguanaduetotheirsize,

anothermotivecanbefangsheng;theBuddhistactofreleasingliveanimalsbelievedto

buildspiritualmerit(NgandLim2010).AsI.iguananativelyoccursinsub-tropicaland

tropicalbiomesidenticaltothosefoundthroughoutsoutheastAsia(Olsonetal.2001),

weexpectcontinuedspreadandgrowthofthesealienpopulationsintheabsenceof

mitigationactions.Indeed,ourcurrentandfutureclimateSDMsindicatethatlargeareas

intheregionhavehighlysuitableI.iguanahabitat.Additionaltoover-landdispersaland

facilitatedbythisspecies’swimandraftcapabilities(Censkyetal.1998;Breuil1999;

vanVeen2011;F.Kraus,pers.comm.2020),throughover-waterdispersalalarge

numberofnovellocationswithsuitablehabitatcouldbereachedfromSingapore(Fig.

2):PeninsularMalaysia,Sumatra,and>3,000islandsoftheIndonesianRiau

archipelago.Intheabsenceofremovalactions,thepersistenceanduncontrolledgrowth

ofI.iguanapopulationsisevidentasnumerouslocationsarewithinhighlysuitable

habitatandrecruitmentispresent(Fig.2).Thecasepresentedherecallsforimmediate

managementactionas1)establishmentstillappearstobeinanearlyphase,2)

eradicationexpensesarerelativelylow,3)currentrecordsarelikelyanunderestimate

asdatawerecollectedopportunisticallybynon-iguanaspecialists,4)alarge

uncontrolledI.iguanapopulationcouldhavefarreachingconsequencesfornative

biodiversity.

Knowledgeontheinvasionpathwayandsourceofalienpopulationsis

importanttopreventrepetitive(un)intentionalincursions.AlthoughI.iguanaisnative

totheAmericantropics,theirimportation,captivebreedingandescapeorrelease

practicescouldleadtounmanageablepopulationgrowthinsoutheastAsia.Between

2000and2017,atotalof1,254liveI.iguanawereimportedintoThailand(importer

9

reportedquantity;CITES2019),thoughcurrentlythenumberofiguanaspresentcould

arguablybehigherduetoincountrycaptivebreedingpracticesaswellasknownimport

discrepanciesinCITESreporting(NijmanandShepherd2011).ForSingapore,542live

specimenshavebeenreportedbyimporterspre-2004(CITES2019),withnorecords

since,likelyduetothecountry’sillegalizationonpetownership.Severalinterviewees

statedthateithertheythemselvesorothers(i.e.,iguanafarms,recreationalparksor

privateresidence)havereleasedcaptiveiguanas.Thiswasinadditiontodeliberate

releasestatementsbysocialmediausers.Increasingthepublicawarenessofthe

negativeeffectsfromIASpopulationsmayhelptodiscouragefuturereleases.

Uncontrolledorflawedexhibitionpracticesofanimalscanleadtotheirescape.

InSpain,Fàbregasetal.(2010)identifiedthatenclosuresecuritywasnotsufficientto

preventescapein14%ofassessedenclosures,mainlyforenclosuresholdingalien

species,whichmightsourceIASpopulations.ForThailand,basedonthepresenceof

free-roamingiguanasclosetoThairecreationalparksthatexhibitnon-cagediguanas,

thesefacilitiesarethemostlikelysourcesofiguanasreportedfromatleasttwoareas:

NakhonSiThammarathandNakhonRatchasima.InSingapore,althoughwedidnot

acquireinformationaboutrecreationalparksthatexhibitfree-roamingiguanas,grounds

ofonepark(JurongBirdPark)areinvadedbyiguanas.Anecdotalevidencesuggeststhat

theirpresenceintheparkandsurroundingareasoriginatesfromtheformer

neighboringreptilerecreationalpark(JurongReptilePark).Inadditiontotheriskof

escapefromparks,free-roamingI.iguanawithinrecreationalparksarereproductively

unhindered,whichleadstonestingandsuccessfulrecruitment.Fromsuchnests,small

freeroaminghatchlingsemergecapableofestablishingoff-groundpopulations.This

posesaparticulardetectionchallenge.Ontopoftheirsmallsize,thelizards’green

colorationallowsthemtoinconspicuouslyblendinwiththefoliage,evadingdetection

foruptoayearintotheirdevelopment.Incontrasttoadults,thesehatchlingsareharder

tocatchandtrackgiventheirsmallsizeandcapacitytodisperse>200mwithinone

monthafterhatching(KnappandAbarca2009).

WithlittleinformationavailableforAsianI.iguanaintroductions,itisnot

possibletomakestraightforwardpredictionsabouttheecologicalimpactsofthese

novelestablishments.Datafromthewesternhemispheredemonstratesthepossibility

thatestablishedpopulationscanspreadpet-tradediseasestonativespecies(Hellebuyk

etal.2017),competitivelydisplacenativespecies(vandenBurgetal.2018b),andcause

erosionanddamagetoagriculturalfields,roadsandairplanes(López-Torresetal.

2011).InThailandwenotethatinvasivepopulationscouldhavethecapacitytodisplace

Physignathuscocincinus,theChinesewaterdragon(IUCNstatusVulnerable;Stuartetal.

10

2019),givenitssmallermaximumsnout-ventlength(SVL)andecologicalnicheoverlap

betweenthespecies.Namely,P.cocincinusisalsoanarboreallizardthatresidescloseto

streamsineastandsoutheasternThailand(Stuartetal.2019).Further,hatchling

iguanaswilllikelybepredatedbynumerousnativespeciesgiventhehighregional

snakediversity(Chan-Ardetal.2015),thoughpredatorsforadultI.iguana(whichcan

reach>45cmSVL)arefew(e.g.largePythonbivittatusorMalayopythonreticulatus

[Lowetal.2016]).Additionally,I.iguanamightcompetewithnativespeciesfor

territory(Chua2007)andnestingsites(e.g.Varanussp.).However,dataonthe

reproductivecycleofI.iguanainSingaporeandThailandiscurrentlylacking,making

reproductiveperiodcomparisonswithnativespeciesdifficult.Nevertheless,imagesof

matingiguanasaswellasareleaseddevelopedeggsuggestmatingoccursaround

November–December.Lastly,highnumbersofalienI.iguanawouldpresumablycause

damagetoagriculturalfields,gardensandplantnurseriesasreportedelsewhere(foran

overviewseeFalcónetal.2013).

Fornaturalareas,over80%ofmangroveplantsinaPuertoRicanareawere

heavilyaffectedbyalienI.iguana(CarloandGarcía-Quijano2008).Asmangrovesare

globallythreatenedandindecline(Polidoroetal.2010),alsoinSingapore(Friessand

Webb2013)despitearecentminorrestoration(Laietal.2015),alienI.iguanaare

expectedtoaggravatethedeclineofSingapore’smangroves.RecordedI.iguana

presenceinSingapore’sSungeiBulohWetlandReserveisthereforeworrisome.Future

surveysandmonitoringarenecessarytobetterunderstandtheecologicalandeconomic

impactofI.iguanaestablishmentinSingaporeandThailand.

AstheglobalpettradehasfacilitatedthespreadofI.iguana,understanding

tradedynamicsmightaidthepredictionoffutureinvasions(Robinsonetal.2015;

Lockwoodetal.2019).AlthoughtheglobalI.iguanatradepeakedintheearly2000’s

(Stephenetal.2011),theimportofliveI.iguanatoAsiawashighestin2015andaclear

declineisabsent(Fig.A2,SupportingInformation).Weproposethatthisstabletrendis

partiallyduetolowershippingcostsandagrowingAsianmiddleclass(Kharas2017).In

additiontoourreport,sightingsofreleasedpetiguanashaveoccurredinTaiwansince

2004whereeradicationactionshavealreadyremoved>2,000I.iguanaindividuals(Lee

etal.2019).Similareradicationactions(plannedorongoing)ofpet-origininvasiveI.

iguanapopulationsareknownfromFijiandGrandCayman(Kraus2019;Rivera-Milán

andHaakonssoninpress).Combiningthesedata,wepredictthe(future)occurrenceof

additionalinvasivealienI.iguanapopulationswithinAsia,specificallyinthePhilippines,

giventheapparenthighoccurrenceofpetI.iguanasfromsocialmediaplatforms,high

numberofCITESimportrecords(Sy2015;CITES2019),aswellaslargeareaswithhigh

11

habitatsuitability(Fig.A3,SupportingInformation).Lastly,therecordsofadultfree-

roamingiguanasfromPeninsularMalaysiaandHongKongarecauseforconcernaswell.

Futureassessmentsshouldidentifywhethertheseareisolatedcasesornot.

Assertiverapidactionisrequiredtohaltthespreadandtosuccessfullyremove

alienI.iguanapopulationsbeforetheybecomeinvasive.Tothatendweprovideseveral

recommendations.First,tomitigatecurrentandfuturenegativeeffectsoftheseI.iguana

invasions,werecommendtheimmediateimplementationofsurveyandquestionnaire

effortstobetterunderstandthespreadofthisspeciesinSingaporeandThailand.We

recommendbothdiurnalandnocturnalsurveyingwherediurnaleffortsmainlyaimto

locateadultandsub-adultspecimensandnocturnalsurveyshatchlingandjuvenile

specimens.Usinghigh-outputheadtorches(e.g.LedLenserH14r.2),small-sizediguanas

canbeeasilylocatedamongfoliagewheretheysleep.Secondly,andinparallel,we

recommendanoutreachcampaigntoraisepublicawareness,inform(future)pet

ownersofalltheconsequencescausedbyreleasingpetiguanasandpromotereporting

ofI.iguanasightingstotherelevant(local)authority.Also,informationshouldbe

providedtonewiguana-petownersuponpurchase,addressingtheincreaseinbody

size,longevity(19.8years[deMagalhãesandCosta2009]),overallexpensesand

necessaryspace.Tostrengthenthis,I.iguanaretailersshouldbeobligatedtoexhibitone

adultindividual(Maceda-Veigaetal.2019),andwerecommendthatretailersofexotic

petsareobligatedtohaveprovenknowledgeofthisspeciesandoftheirexhibition

standards.Thirdly,werecommendinspectionsofI.iguanacaptivitycircumstancesfor

allfacilitieswherethisspeciesiskept;forexample,zoos,recreationalparksandiguana

farms.Iguanasshouldnotbeallowedtoroamfreely,butinsteadbeexhibitedinlarge

cagesorsmall-sizedopenareasenclosedbyadeeptrenchwithasmoothmetallic

verticalsurfacetopreventclimbing;treebranchesfromwithintheexhibitionarea

shouldnotextendbeyondthistrench.Importantly,enclosureorentrapmentbywateris

ineffectivegiventheswimmingcapacityofI.iguana.Lastly,werecommendthat

releasingapetI.iguanabeimmediatelyprohibitedbylawinThailand,althoughdespite

itsprohibitioninSingaporethepracticecontinues(NgandLim2010).Petrelease

preventioncouldbeassistedbypittaggingallimportedandin-countrybrediguanasto

identifyregisteredowners.Besidestheabovementionedactions,additionalcountry

specificeffortsarenecessaryduringthisearlyestablishmentphaseinordertoprevent

futuremulti-milliondollareradicationefforts.

ConflictofInterest:Theauthorsdeclarethattheyhavenoconflictofinterest.

12

DataAccessibility

TheRscriptanddatatorunSDMmodelsasmentionedinourMethodsandMaterials

areavailablethroughGitHub;github.com/StevenVB12/SDM_Iguana.

Acknowledgements

WearegratefultoallcontributorsforsharingdataonIguanaiguanasightings.Andwish

tothankJasonKolbeforimprovinganolderversionofthismanuscript.

References

1. BlackburnTM,PyšekP,BacherSetal(2011)Aproposedunifiedframeworkfor

biologicalinvasions.TrendsEcolEvolut26:333–339

2. BockB,MaloneC,KnappC,AparicioJetal(2018)Iguanaiguana.TheIUCNRed

ListofThreatenedSpecies2018:e.T174481A1414646.

3. BoonkuawP,KanchanasakaB,PrayoonU(2014)Thedistributionofalienfauna

inThailand.WildlifeYearbook14:103–126

4. BoriaRA,OlsonLE,GoodmanSM,AndersonRP(2014)Spatialfilteringtoreduce

samplingbiascanimprovetheperformanceofecologicalnichemodels.Ecol

Model275:73–77

5. BreuilM(1999)Editorial.WestIndianIguanaSpecialistGroupNewsletter2:4

6. BriscoeRunquistRD,LakeT,TiffinPetal(2019)Speciesdistributionmodels

throughouttheinvasionhistoryofPalmeramaranthpredictregionsatriskof

futureinvasionandrevealchallengeswithmodelingrapidlyshiftinggeographic

ranges.SciRep9:2426

7. CarloTA,García-QuijanoCG(2008)Assessingecosystemandculturalimpactsof

thegreeniguana(Iguanaiguana)invasionintheSanJuanBayEstuary(SJBE)in

PuertoRico.FinalReporttotheSanJuanBayEstuaryProgram,SanJuan,Puerto

Rico

8. CenskyEJ,HodgeK,DudleyJ(1998)Over-waterdispersaloflizardsdueto

hurricanes.Nature395:556

9. Chan-ArdT,ParrJWK,NabhitabhataJ(2015)Afieldguidetothereptilesof

Thailand.NewYork:OxfordUniversityPress

10. ChatterjeeS,HadiAS(2006)Regressionanalysisbyexample.NewYork,John

Wiley&Sons

11. ChewI,LowM-R(2017)RoadkillgreeniguanaatUpperThomson.Singapore

BiodiversityRecords2017:5

13

12. ChuaEK(2007)FeralIguanaattacksVaranussalvatoratSungeiBulohWetland

Reserve.Biawak1:35–36

13. CITES(2019)CITEStradestatisticsderivedfromtheCITESTradeDatabase.

UNEPWorldConservationMonitoringCentre,Cambridge,UK

14. DavisMA(2009)InvasionBiology.OxfordUniversityPress,Oxford,UK

15. ElithJ,KearneyM,PhillipsSJ(2010)Theartofmodellingrange-shiftingspecies.

MethodEcolEvol1:330–342

16. EngemanR,JacobsonE,AveryML,MeshakaWEJr(2011)Theaggressive

invasionofexoticreptilesinFloridawithafocusonprominentspecies:areview.

CurrBiol57:599–612

17. FàbregasMC,Guillén-SalazarF,Garcés-NarroC(2010)Theriskofzoological

parksaspotentialpathwaysfortheintroductionofnon-indigenousspecies.Biol

Invasions12:3627–3636

18. FalcónW,AckermanJD,DaehlerCC(2012)MarchoftheGreenIguana:non-

nativedistributionandpredictedgeographicrangeofIguanaiguanainthe

GreaterCaribbeanregion.IRCFReptilesAmphib19:150–160

19. FalcónW,AckermanJD,RecartW,DaehlerCC(2013)Biologyandimpactsof

Pacificislandinvasivespecies.10.Iguanaiguana,thegreeniguana(Squamata:

Iguanidae).PacSci67:157–186

20. FickSE,HijmansRJ(2017)Worldclim2:New1-kmspatialresolutionclimate

surfacesforgloballandareas.IntJClimatol37:4302–4315

21. FriessDA,WebbEL(2013)Variabilityinmangrovechangeestimatesand

implicationsfortheassessmentofecosystemserviceprovision.GlobalEcol

Biogeogr23:715–725

22. GBIF.org(2019)GBIFoccurrencedownload.

https://doi.org/10.15468/dl.exm8hhAccessed06November2019.

23. HellebuyckT,QuestelK,PasmansF,vanBrantegemL,PhilipP,MartelA(2017)

AvirulentcloneofDevrieseaagamarumaffectsendangeredLesserAntillean

iguanas(Iguanadelicatissima).SciRep7:12491

24. HijmansRJ,PhillipsS,LeathwickJ,ElithJ(2017)dismo:speciesdistribution

modeling.Rpackageversion1.1-4.https://CRAN.R-project.org/package=dismo

25. KharasH(2017)Theunprecedentedexpansionoftheglobalmiddleclass:an

update.GlobalEconomyandDevelopmentworkingpaper100.BrookingsIndia.

http://hdl.handle.net/11540/7251

26. KhooMDY(2016)GreeniguanasatKranjiReservoir.SingaporeBiodiversity

Records2016:185

14

27. KnappCR,AbarcaJG(2009)Effectsofradiotransmitterburdeningonlocomotor

abilityandsurvivalofiguanahatchlings.Herpetologica65:363–372

28. KolbeJJ,GlorRE,SchettinoLR,LaraAC,LarsonA,LososJB(2004)Genetic

variationincreasesduringbiologicalinvasionbyaCubanlizard.Nature

431:177–181

29. KrausF(2019)EradicationplanforGiantInvasiveIguana(Iguanaiguana)in

Fiji.ReportpreparedforUnitedNationsDevelopmentProgram,Suva

30. LaiS,LokeLHL,HiltonMJ,BoumaTJ,ToddPA(2015)Theeffectsofcoastal

urbanizationoncoastalhabitatsandthepotentialforecologicalengineering:a

Singaporecasestudy.OceanCoastManage103:78–85

31. LeeK-H,ChenT-H,ShangG,ClulowS,YangY-J,LinS-M(2019)Achecklistand

populationtrendsofinvasiveamphibiansandreptilesinTaiwan.ZooKeys

829:85–130

32. LockwoodJL,WelbourneDJ,RomagosaCM,CasseyP,etal.(2019)Whenpets

becomepests:theroleoftheexoticpettradeinproducinginvasivevertebrate

animals.FrontEcolEnviron17:323–330

33. López-TorresAL,Claudio-HernándezHJ,Rodríguez-GómezCA,LongoAV,Joglar

RL(2012)Greeniguanas(Iguanaiguana)inPuertoRico:isittimefor

management?BiolInvasions14:35–45

34. LowM-R,BickfordDP,TanM,NevesLC(2016)Malayopythonreticulatus

(Reticulatedpython).Diet.HerpetolRev47:148–149

35. Maceda-VeigaA,Escribano-AlacidJ,Martínez-SilvestreA,VerdaguerI,MacNally

R(2019)What’snext?Thereleaseofexoticpetscontinuesvirtuallyunabated7

yearsafterenforcementofnewlegislationformanaginginvasivespecies.Biol

Invasions21:29–33

36. deMagalhãesJP,CostaJ(2009)Adatabaseofvertebratelongevityrecordsand

theirrelationtootherlife-historytraits.JEvolBiol22:1770–1774

37. MitoT,UesugiT(2004)InvasivealienspeciesinJapan:Thestatusquoandthe

newregulationforpreventionoftheiradverseeffects.GlobEnvironRes8:171–

191

38. MossJB,WelchME,BurtonFJ,ValleeMV,HoulcroftEW,LaaserT,GerberGP

(2017)FirstevidenceforcrossbreedingbetweeninvasiveIguanaiguanaandthe

nativerockiguana(GenusCyclura)onLittleCaymanIsland.BiolInvasions

20:817–823

39. NaimiB,AraújoMB(2016)sdm:areproducibleandextensibleRplatformfor

speciesdistributionmodelling.Ecography39:368–375

15

40. NgTH,LimKKP(2010)IntroducedaquaticherpetofaunaofSingapore’s

reservoirs.Cosmos6:117–127

41. NgBC,LimKKP(2015)GreeniguanaatSungeiTengah.SingaporeBiodiversity

Records2015:51

42. NijmanV(2010)AnoverviewofinternationalwildlifetradefromSoutheast

Asia.BiodiversConserv19:1101–1114

43. NijmanV,ShepherdCR(2007)Tradeinnon-native,CITES-listed,wildlifeinAsia,

asexemplifiedbythetradeinfreshwaterturtlesandtortoises(Chelonidae)in

Thailand.ContribZool76:207–211

44. NijmanV,ShepherdCR(2010)TheroleofAsiaintheglobaltradeinCITESII-

listedpoisonarrowfrogs:hoppingfromKazakhstantoLebanontoThailandand

beyond.BiodivConserv19:1963–1970

45. NijmanV,ShepherdCR(2011)TheRoleofThailandintheInternationalTradein

CITES-ListedLiveReptilesandAmphibians.PLoSONE6:e17825

46. NijmanV,ToddM,ShepherdCR(2012)Wildlifetradeasanimpedimentto

conservationasexemplifiedbythetradeinreptilesinSoutheastAsia.Biotic

EvolutionandEnvironmentalChangeinSoutheastAsia.Eds.GowerDJetal.Pp

391–405.CambridgeUniversityPress.

47. OlsonDM,DinersteinE,WikramanayakeED,BurgessND,etal.(2001)

Terrestrialecoregionsoftheworld:anewmapoflifeonEarth.BioScience

51:933–938

48. PhilipsSJ,DudíkM,SchapiremRE(2018)MaxEntsoftwareformodelingspecies

nichesanddistributions.

http://biodiversityinformatics.amnh.org/open_source/maxent/.Accessed16

October2019.

49. PolidoroBA,CarpenterKE,CollinsL,DukeNC,etal.(2010)Thelossofspecies:

mangroveextinctionriskandgeographicareasofglobalconcern.PLoSONE5:

e10095

50. PooleCM,ShepherdCR(2017)Shadesofgrey:thelegaltradeinCITES-listed

birdsinSingapore,notablythegloballythreatenedAfricangreyparrotPsittacus

erithacus.Oryx51:411–417

51. RCoreTeam(2019)ALanguageandEnvironmentforStatisticalComputing.

Version3.5.1.Availableatwww.R-project.org/.

52. Rivera-MilánFF,HaakonssonJ(inpress)Monitoring,modelingandharvest

managementofnon-nativeinvasiveGreeniguanasonGrandCayman,Cayman

Islands.BiolInvasions.

16

53. RobinsonJE,GriffithsRA,StJohnFAV,RobertsDL(2015)Dynamicsoftheglobal

tradeinlivereptiles:Shiftingtrendsinproductionandconsequencesfor

sustainability.BiolConserv184:42–50

54. StephenC,PasachnikS,ReuterA,MosigP,RuyleL,FitzgeraldL(2011)Surveyof

status,trade,andexploitationofCentralAmericaniguanas.Report,Department

ofInterior,UnitedStatesFishandWildlifeService,Washington,D.C.

55. StephenCL,ReynosoVH,CollettWS,HasbunCR,BreinholtJW(2013)

Geographicalstructureandcrypticlineageswithincommongreeniguanas,

Iguanaiguana.JBiogeogr40:50–62

56. StuartB,SumonthaM,CotaM,PanitvongN,NguyenTQ,Chan-ArdT,NeangT,

RaoD-Q,YangJ(2019)Physignathuscocincinus.TheIUCNRedListof

ThreatenedSpecies2019:e.T104677699A104677832.

57. SwetsJA(1988)Measuringtheaccuracyofdiagnosticsystems.Science

240:1285–1293

58. SyEY(2015)ChecklistofexoticspeciesinthePhilippinepettrade,II.reptiles.J

NatureStudies14:66–93

59. TayJB(2015)GreeniguanaatBurgundyCrescent.SingaporeBiodiversity

Records2015:188

60. vandenBurgMP,MeirmansPG,vanWagensveldTP,KluskensB,MaddenH,

WelchME,BreeuwerJAJ(2018a)TheLesserAntilleanIguana(Iguana

delicatissima)onSt.Eustatius:geneticallydepauperateandthreatenedby

ongoinghybridization.JHered109:426–437

61. vandenBurgM,BreuilM,KnappC(2018b)Iguanadelicatissima.TheIUCNRed

ListofThreatenedSpecies2018:e.T10800A122936983.

62. vandenBurgMP,BrisbaneJLK,KnappCR(2020)Post-hurricanerelieffacilitates

invasionandestablishmentoftwoinvasivealienvertebratespeciesinthe

CommonwealthofDominica,WestIndies.BiolInvasions22:195–203

63. vanVeenR(2011)StatusReport:TheAmericanIguana(Iguanaiguana)inFiji:

May-August2011.ReportpreparedforNatureFiji-MareqetiVitiandthe

AmericanIguanaEradicationTaskForce.

64. vanWagensveldTP,vandenBurgMP(2018)Firstrecordonfecundityofan

Iguanahybridanditsimplicationsforconservation:evidenceforgenetic

swampingbynon-nativeiguanas.HerpetolNotes11:1079–1082

65. VuillaumeB,ValetteV,LepaisO,GrandjeanF,BreuilM(2015)Geneticevidence

ofhybridizationbetweentheendangerednativespeciesIguanadelicatissima

17

andtheinvasiveIguanaiguana(Reptilia,Iguanidae)intheLesserAntilles:

managementimplications.PLoSONE10:e0127575

66. YeoJWL(2014)GreeniguanaatKovan.SingaporeBiodiversityRecords

2014:119

67. YeoRKH(2019)AgreeniguanaattheBotanicGardens.SingaporeBiodiversity

Records2019:38

68. YeoDCJ,ChiaCSW(2010)IntroducedspeciesinSingapore:anoverview.Cosmos

6:23–37

18

Supplementarymaterials

Fig.A1SpeciesdistributionmodelforIguanaiguanainSingapore,Thailandandsurroundingcountriesfor2050withtheACmodelandrcp45forgreenhousegasemission(FickandHijmans2017).Modelsusedanabsencethresholdof0.15andhabitatsuitabilityrangesfromhigh(darkred)tolow(white).BluedotsrepresentlocationswithI.iguanapresence.

19

Fig.A2ReportedCITESimportsofIguanaiguanatoAsiancountriesbetween2000–2017(CITESDatabase2019)

20

Fig.A3Speciesdistributionmodel(ashabitatsuitability)forIguanaiguanainPhilippinesundercurrentclimate,withabsencethreshold0.17.Habitatsuitabilityrangesfromhigh(darkred)tolow(white).

21

TableA1IguanaiguanasightingsinThailandandSingaporeincludinglocation,year,

numberofindividuals,andlifestage(s)present

Country Location GPS Year Individuals Life

stage(s)

Singapore SungeiTengahRoad 1.38075,

103.73031

2013,

2019

3 juvenile

andadult

Singapore JalanRengkam 1.36246,

103.88880

2014 1 subadult

Singapore JurongBirdPark,and

JurongHill

1.31950,

103.70503

2015,

2016,

2017,

2018,

2019

>20 all

Singapore BurgundyCrescent 1.34017,

103.76145

2015 1 subadult

Singapore SungeiPengSiang 1.3937,

103.7254

2016 2 adult

Singapore OldUpperThomson

Road

1.38030,

103.81884

2017 1 subadult

Singapore JapaneseGardens 1.33522,

103.73136

2018 2 adult

Singapore TanahMerah 1.32096,

103.96723

2018 1 juvenile

Singapore OldChuaChuKang 1.38,103.74 2018 2 adult

Singapore WarrenCountryClub 1.38500,

103.73411

2018,

2019

>10 juvenile

andadult

Singapore Temenggong

RoadMosque

1.2665,

103.8244

2018 1 adult

Singapore PasirRisPark 1.3794,

103.9503

2018 1 adult

Singapore JurongEcoGarden 1.35228,

103.69319

2018 1 adult

Singapore Serangoonarea 1.3554,

103.8632

2018 1 juvenile

Singapore BotanicGarden 1.31185, 2019 1 subadult

22

103.81609

Singapore YishunPond 1.42646,

103.84024

2019 1 adult

Singapore SengKangPcn 1.38602,

103.90940

2019 1 adult

Thailand KhaoYai

NationalPark

14.44932,

101.40164

2016 1 adult

Thailand NakhonRatchasima 14.85005,

102.07593

2016,

2017

7 adultand

juvenile

Thailand Sakaerat 14.48468,

101.92032

2017 1 adult

Thailand HuaHin 12.58,99.93 2018,

2019

3 adult

Thailand KaengKrachan

reservoir

12.91098,

99.61502

2019 1 adult

Thailand Korat 14.88712,

102.188312

2019 1 subadult

Thailand NakhonSi

Thammarath

8.4574,

99.9539

2019 >20 subadult

andadult

Thailand Ubonrat 16.77,102.71 2019 >30 subadult

andadult

Thailand Phattaya 12.86231,

100.96929

2019 6 adultand

juvenile

Thailand UthaiThanidistrict 15.42,99.74 2019 >20 adultand

hatchling

Thailand BanPongRatchaburi 13.81175,

99.86228

2019 5–20 adultand

hatchling

Thailand NattawutNambut 16.29974,

103.98282

2019 2 adult