Divergent habitat use of two urban lizard speciesEcology and Evolution. 2018;8:25–35. | 25...
11
Ecology and Evolution. 2018;8:25–35. | 25 www.ecolevol.org Received: 7 June 2017 | Revised: 1 September 2017 | Accepted: 11 October 2017 DOI: 10.1002/ece3.3600 ORIGINAL RESEARCH Divergent habitat use of two urban lizard species Kristin M. Winchell 1 | Elizabeth J. Carlen 2 | Alberto R. Puente-Rolón 3 | Liam J. Revell 1,4 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 1 Department of Biology, University of Massachusetts Boston, Boston, MA, USA 2 Department of Biology, Fordham University, Bronx, NY, USA 3 Departamento de Biología, Universidad de Puerto Rico, Mayagüez, PR, USA 4 Programa de Biología, Universidad del Rosario, Bogotá, Colombia Correspondence Kristin M. Winchell, Department of Biology, University of Massachusetts Boston, Boston, MA, USA. Email: [email protected] Funding information Directorate for Biological Sciences (National Science Foundation), Grant/Award Number: 1354044 Abstract Faunal responses to anthropogenic habitat modification represent an important aspect of global change. In Puerto Rico, two species of arboreal lizard, Anolis cristatellus and A. stratulus, are commonly encountered in urban areas, yet seem to use the urban habi- tat in different ways. In this study, we quantified differences in habitat use between these two species in an urban setting. For each species, we measured habitat use and preference, and the niche space of each taxon, with respect to manmade features of the urban environment. To measure niche space of these species in an urban environ- ment, we collected data from a total of six urban sites across four different municipali- ties on the island of Puerto Rico. We quantified relative abundance of both species, their habitat use, and the available habitat in the environment to measure both micro- habitat preference in an urban setting, as well as niche partitioning between the two different lizards. Overall, we found that the two species utilize different portions of the urban habitat. Anolis stratulus tends to use more “natural” portions of the urban envi- ronment (i.e., trees and other cultivated vegetation), whereas A. cristatellus more fre- quently uses anthropogenic structures. We also found that aspects of habitat discrimination in urban areas mirror a pattern measured in prior studies for forested sites in which A. stratulus was found to perch higher than A. cristatellus and preferred lower temperatures and greater canopy cover. In our study, we found that the multi- variate niche space occupied by A. stratulus did not differ from the available niche space in natural portions of the urban environment and in turn represented a subset of the niche space occupied by A. cristatellus. The unique niche space occupied by A. cris- tatellus corresponds to manmade aspects of the urban environment generally not uti- lized by A. stratulus. Our results demonstrate that some species are merely tolerant of urbanization while others utilize urban habitats in novel ways. This finding has implica- tions for long-term persistence in urban habitats and suggests that loss of natural habi- tat elements may lead to nonrandom species extirpations as urbanization intensifies. KEYWORDS anole, Anolis cristatellus, Anolis stratulus, niche partitioning, Puerto Rico, urbanization 1 | INTRODUCTION Urbanization is one of the greatest sources of habitat change in the modern era. Urban areas occupy a large and expanding fraction of the landscape worldwide and are expected to increase in extent and in- tensity in coming years (Forman, 2014; United Nations 2012). Which species can tolerate this urbanization and how they achieve that end is an increasingly important aspect of ecology in an era of global change.
Transcript of Divergent habitat use of two urban lizard speciesEcology and Evolution. 2018;8:25–35. | 25...
Ecology and Evolution 2018825ndash35 emsp|emsp25wwwecolevolorg
Received7June2017emsp |emsp Revised1September2017emsp |emsp Accepted11October2017DOI101002ece33600
O R I G I N A L R E S E A R C H
Divergent habitat use of two urban lizard species
Kristin M Winchell1 emsp|emspElizabeth J Carlen2emsp|emspAlberto R Puente-Roloacuten3emsp|emspLiam J Revell14
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2017TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd
1DepartmentofBiologyUniversityofMassachusettsBostonBostonMAUSA2DepartmentofBiologyFordhamUniversityBronxNYUSA3DepartamentodeBiologiacuteaUniversidaddePuertoRicoMayaguumlezPRUSA4ProgramadeBiologiacuteaUniversidaddelRosarioBogotaacuteColombia
CorrespondenceKristinMWinchellDepartmentofBiologyUniversityofMassachusettsBostonBostonMAUSAEmailkristinwinchell001umbedu
Funding informationDirectorateforBiologicalSciences(NationalScienceFoundation)GrantAwardNumber1354044
AbstractFaunalresponsestoanthropogenichabitatmodificationrepresentanimportantaspectofglobalchangeInPuertoRicotwospeciesofarboreallizardAnolis cristatellusandA stratulusarecommonlyencounteredinurbanareasyetseemtousetheurbanhabi-tatindifferentwaysInthisstudywequantifieddifferencesinhabitatusebetweenthesetwospeciesinanurbansettingForeachspecieswemeasuredhabitatuseandpreferenceandthenichespaceofeachtaxonwithrespecttomanmadefeaturesoftheurbanenvironmentTomeasurenichespaceofthesespeciesinanurbanenviron-mentwecollecteddatafromatotalofsixurbansitesacrossfourdifferentmunicipali-tiesontheislandofPuertoRicoWequantifiedrelativeabundanceofbothspeciestheirhabitatuseandtheavailablehabitatintheenvironmenttomeasurebothmicro-habitatpreferenceinanurbansettingaswellasnichepartitioningbetweenthetwodifferentlizardsOverallwefoundthatthetwospeciesutilizedifferentportionsoftheurbanhabitatAnolis stratulustendstousemoreldquonaturalrdquoportionsoftheurbanenvi-ronment(ietreesandothercultivatedvegetation)whereasA cristatellusmorefre-quently uses anthropogenic structures We also found that aspects of habitatdiscriminationinurbanareasmirrorapatternmeasuredinpriorstudiesforforestedsitesinwhichA stratuluswasfoundtoperchhigherthanA cristatellusandpreferredlowertemperaturesandgreatercanopycoverInourstudywefoundthatthemulti-variate niche space occupied byA stratulus did not differ from the available nichespaceinnaturalportionsoftheurbanenvironmentandinturnrepresentedasubsetofthenichespaceoccupiedbyA cristatellusTheuniquenichespaceoccupiedbyA cris-tatelluscorrespondstomanmadeaspectsoftheurbanenvironmentgenerallynotuti-lizedbyA stratulusOurresultsdemonstratethatsomespeciesaremerelytolerantofurbanizationwhileothersutilizeurbanhabitatsinnovelwaysThisfindinghasimplica-tionsforlong-termpersistenceinurbanhabitatsandsuggeststhatlossofnaturalhabi-tatelementsmayleadtononrandomspeciesextirpationsasurbanizationintensifies
K E Y W O R D S
anoleAnolis cristatellusAnolis stratulusnichepartitioningPuertoRicourbanization
1emsp |emspINTRODUCTION
Urbanization isoneofthegreatestsourcesofhabitatchange inthemoderneraUrbanareasoccupyalargeandexpandingfractionofthe
landscapeworldwideandareexpectedto increase inextentandin-tensityincomingyears(Forman2014UnitedNations2012)Whichspeciescantoleratethisurbanizationandhowtheyachievethatendisanincreasinglyimportantaspectofecologyinaneraofglobalchange
26emsp |emsp emspensp WINCHELL Et aL
Amajor consequence of urbanization is the filtering of speciesoften resulting in lower biodiversity such that a subset of the orig-inal native community is represented in theurbanhabitat (Aronsonetal2014Forman2014)Ingeneralurbancommunitiesaredomi-natedbyurban-tolerantspecieswithabundancesdecliningasurban-izationincreasesanddiversitydecliningascitiesage(Forman2014GrantMiddendorfColganAhmadampVogel2011McKinney2008ShochatWarrenFaethMcIntyreampHope2006)Howeverurbaniza-tioncangeneratenovelhabitatspaceundersomecircumstancesre-sultinginnewecologicalopportunitiesandspeciescolonizationWhilethismay leadtoenhancedabundanceanddiversity theseadditionstypicallyconsistofnonnativespecies(McKinney2002Shochatetal2006)Nonethelessurbanareascanstillsupportsubstantialbiodiver-sity(Forman2014)
Some species are able to adapt to changes associatedwith ur-banization (eg Harris Munshi-South Obergfell amp OrsquoNeill 2013Winchell Reynolds Prado-Irwin Puente-Roloacuten amp Revell 2016)Speciesthatpersistinurbanhabitatstendtohaveseveralcharacteris-ticsincommonbroadhabitatanddietrequirements(generalists)highmobilitylargereproductiveoutputsmallbodysizeandtoleranceofhumandisturbances(Grantetal2011)Yetdifferencesintolerancesandpreferencesbetweenspeciesmeanthatnotallspeciesareabletosimilarlymeettheirneedsinurbanenvironments
Animalsthatpersistinurbanareasfaceamodifiedhabitatdom-inated by human structures lacking continuous canopy cover andexhibitingdifferentthermalandhydrologicconditionsfromthoseofnaturalareasnearby(reviewedinForman2014)Somespeciespersistinurbanareasbutarestilldependentonnearbynaturalareastomain-tainpositivepopulationgrowthSuchspeciesareoftenreferredtoasldquotolerantrdquo or ldquourban adaptersrdquo (McKinney 2002) By contrast otherspeciesfoundinurbanhabitatshavefullyembracedtheirnewfoundmilieu utilize anthropogenic resources extensively and may evenachievehigherpopulationgrowthratesanddensities inurbanareasthanatnaturalsitesThesespeciesarereferredtoasldquosynanthropicrdquoldquourbanophilicrdquoorldquourbanexploitersrdquo(Forman2014Grantetal2011McKinney2006)
For urbanophiles urbanization may have created a preferablehabitatwhencomparedtotheirhistoricnaturalareawithabundantfoodrefugesandaccesstomatesForexampleanthropogenicwastealongwithinsectsattractedtothiswasteandtoartificiallightsourcesmayincreasetheavailabilityoffoodonlocalscalesforinsectivorousherpetofauna (Henderson amp Powell 2001 Perry Buchanan FisherSalmonampWise2008)Shochatetal(2010)foundthatelevatedden-sitiesofsomeurbanbirdspeciescanbeattributedtobothbottom-up(more food resources) and top-down (relaxed predation) controlsUrbanophilicspeciesnotonlypersist inurbanhabitatsbutalsotakefulladvantageofthenovelenvironmentanditsresourceseffectivelyexpandingintothenewnichespacethatcanbeassociatedwithman-madestructuresandresources
Puerto Rico provides an excellent opportunity to study animalresponses to long-term and intensifying human-modification of theenvironment Human settlement of the island by indigenous peo-ples began 5000years before the present day andwas succeeded
by intensive European settlement beginning in the early 16th cen-turyTheseerasof colonizationhave resulted in successiveperiodsof intensehabitatmodification InparticularPuertoRicowasnearlycompletelydeforestedforthepurposesofagricultureThisperiodofdeforestationpeakedinthe1940swhenaslittleas6forestcoverremainedontheisland(Koenig1953MillerampLugo2009)Overthepastsevendecadesforestcoverhasprogressivelyregeneratedasag-ricultural lifestyleswere abandoned and industrialization increasedbut this has been concurrentwith an expansion and intensificationof urban development island-wide (Martinuzzi Gould amp RamosGonzaacutelez2007MillerampLugo2009)Thenetresultofthisdeclineinagriculturalandincreaseinindustrializationhasbeenadramaticriseintheextentofurbanareasbyanestimated42infewerthantwodecades(Helmer2004LoacutepezAideampThomlinson2001)
Presentlyurbanareascover11oftheislandandcontinuetointensifyinspatialextentandpopulationdensity(Martinuzzietal2007MillerampLugo2009USCensusBureau2012)Urbanareasarecharacterizedbylargepercentagesofimpervioussurfaces(egroadsconcrete)andlowlevelsofvegetativecanopycoverWithapopulationof3725789(938ofwhichresideinurbanareasUSCensusBureau2012)PuertoRicorsquosurbanareasincludelow-densityurbanization (suchas ruralcommunities)midsizecitiesdominatedby suburban communities and sprawlingmetropolitan areaswithlittle tono remainingnaturalhabitat andmore thanamillion res-idents(egMetropolitanSanJuan)This intenselandmodificationand the pressures associatedwith human presence have resultedinadeclineofmanynativeplantandanimalspecies(Koenig1953MillerampLugo2009)Despitethiscenturies-longprocessofurban-ization many native Puerto Rican species persist in and aroundurbansites
ThePuertoRicanCrestedAnoleAnolis cristatellusandtheBarredAnoleAnolis stratulus(Figure1)areperhapsthemostcommonurbananolespeciesinPuertoRicoandaretheonlytwowehaveregularlyobservedinvirtuallyalltypesofurbanareasisland-wideBothspeciesare relatively small arboreal lizards (adultmale SVL 50ndash75mm and35ndash55mm respectively)Anoles are characterized by the repeatedindependentevolutionofecologicallyandmorphologicallysimilarmi-crohabitatspecialists(ldquoecomorphsrdquo)ondifferentislandsAmongtheseAnolis cristatellusiscategorizedasaldquotrunk-groundrdquospecialistwhereasA stratulusisaldquotrunk-crownrdquospecialist(Losos2009)Thesedesigna-tionsaredefinedbybothhabitatuseandmorphologyTrunk-groundanolessuchasA cristatellusarebrownincolorhaverelativelylonglimbsastockybuildandperchlowtothegroundonbroadsurfacessuchastreetrunksIncontrasttrunk-crownanolessuchasA stratu-lusaretypicallygreenincolor(althoughA stratulusislightgray)haverelativelyshort limbsaremoreslenderandperchfromeye-level tohighupintreesutilizingleavestwigsbranchesandtrunksasperches(reviewedinLosos2009)
Anolis cristatellusandA stratulusarefoundatlowerelevationsandinbothmesicandxerichabitatswheretheyexperiencehighertem-peratureandlowerhumiditycomparedtomanyuplandspecieswithmorestrictthermalrequirements(Rand1964)Thusitisperhapsun-surprisingthatbothspeciesaretolerantofurbanhabitatwhichtends
emspensp emsp | emsp27WINCHELL Et aL
to be warmer and drier than nearby forests (reviewed in Forman2014)Wherethetwospeciesco-occurinnaturalforesthabitatstheypartitionthehabitatstructurallyandclimaticallySpecificallypriorre-search suggests thatA stratulus utilizeshigher and thinnerperchesandperchsitesthatarecoolerhigherinhumidityandhavemoreex-tensivecanopycovercomparedtohabitatusedbyA cristatellus(Rand1964Reagan1992)
Hereweaskhowthesetwospeciesutilizeandpartitionanovelhabitat urban areas Our null hypothesis is that theywill maintainniche partitioning and habitat choices in the samemanner as theydointhenaturalforesthabitatschoosingnaturalsubstratesthatfittheirpreferencesInotherwordsA stratuluswillseekouthigherthin-nercoolerpercheswiththickercanopycoverwhileA cristatellus will seekoutlowerbroaderwarmerpercheswiththinnercanopycoverAlternativelybothspeciesmayutilize thenovelnichespaceassoci-atedwithmanmadehabitat(ieonandaroundbuildings)Athirdpos-sibilityisthatonlyonespeciesexpandsintothenovelhabitatspaceassociated with anthropogenic resources while the other remainsstrictlyassociatedwithnaturalaspectsoftheurbanspace
WetestedthesehypothesesbymeasuringtherelativeabundancehabitatuseandnichespaceoccupiedbythesetwospeciesinurbanareasBecauseA cristatellus ismoreofageneralistwepredict thatitwilloccupyagreaterportionoftheurbanhabitatspaceandmoreextensively utilize habitat associatedwith anthropogenic structureswhile A stratuluswillremainassociatedwithnaturalhabitatelementsSimilartonaturalhabitatswealsopredictthateachspecieswillnon-randomlyutilizeperchesthatbestmeettheirstructuralandclimaticpreferencesasobserved innatural areasUnderstandingdifferentialhabitatuseinurbanpersistentspeciesshedslightonthefactorsinflu-encingurbantolerance(thegeneralcapacitytopersistinurbanareas)versusgenuineurbanophilyHereweprovideanempiricaltestofthisecological theoryMoreover this typeofnaturalhistory informationcanaidconservationinurbanareasbyidentifyingtheminimumhab-itat requirementsofnative species and thepotential forurbanper-sistenceandadaptation
2emsp |emspMATERIALS AND METHODS
From24April2015to6May2015wesampledsixurbansitesinfourmunicipalitiesinnorthernandwesternPuertoRicoSanJuanAreciboAguadilla and Mayaguumlez (Figure2a) In San Juan Aguadilla andMayaguumlez thesiteswereresidentialneighborhoods InArecibowesampledoneresidentialneighborhoodandtwouniversitycampuses(UniversityofPuertoRicoAreciboandUniversityInteramericana)ForlogisticalreasonswedidnotsamplenearbyforestedareasOurvisualsamplingmethodsusedintheurbanhabitatwouldlikelyhavebeenin-adequateinforesthabitatsduetothedifferencesinstructuralhabitatcomplexityandcanopyusebyA stratulus
Ateachlocalitywesampledabundancebyslowlywalkingthroughthehabitatforaminimumof3hrwithoutretracingourpathbetween8amand7pm(dusk)Becausethesespeciesvaryintheirhabitatusethroughoutthedayinnaturalforesthabitats(Hertz1992Nicholsonetal2005)andinurbanhabitats(Avileacutes-Rodriacuteguezunpublished data)surveyswereconductedatdifferenttimesofthedaywithatleastonesite surveyedduring each daylight hour (Figure2b) For every adultlizardobservedwerecordedspeciesandperchsubstrate
Wechosea subsetof theobserved lizardsas focalanimalsWeonlychosefocalanimalsoccupyinguniqueperchestoavoidaccidentalpseudoreplication(iewedidnotsamplemultiplelizardsofthesame
F IGURE 1emspAnolis cristatellus(topphotoEJC)andAnolis stratulus (bottomphotoKMW)occupydifferentportionsoftheurbanhabitat
(a)
(b)
28emsp |emsp emspensp WINCHELL Et aL
speciesutilizingthesametree)BecauseofdifferencesinabundancewesampledeveryA stratulusoccupyingauniqueperchandthenextobservedA cristatellus resulting inapproximatelyequalnumbersoffocalobservationsperspeciesForfocalanimalswenotedenviron-mentalconditionsandhabitatuseambienttemperature(digitalprobeOMEGAHH12B)perchtemperature(infraredprobeEXTECHIR201)relativehumidity(digitalmeterAMPROBETHWD-3)sunconditionsperchheightperchdiameterdistancetonearestpotentialperch(anystructureatleast05mhighandrobustenoughtosupporttheweightofanadultofeitherspecies)perchtypeandperchroughnessPerchroughnesswasratedonascaleof1ndash5withlowernumbersindicatingsmoothersubstratesRatingswereasfollows(basedonpreviousanal-ysesofsurfaceroughnessandsubstratetypeWinchelletal2016)(1)glass(2)metal(3)paintedconcrete(4)unpaintedprocessedwoodleaves and smooth bark trees such as bamboo and (5) thick barktreessuchasTababuya amarilloandCalophyllum antillanumaswellasunpainted andweathered concreteWe took photos of the canopyimmediatelyabovetheperchsite(OlympusEP5withOlympus9mm180fisheye)Weestimatedvegetativecanopycoverandmanmadecanopycover(iemanmadestructuresobscuringthesky)fromthesephotographsusingAdobePhotoshop(CS51)
Foreveryfocalanimalwealsosampledavailablehabitatbyran-domlyselectinganearbyperchWesamplednearbyavailableperchesbychoosingtheclosestpotentialperchinarandomdirectionfromthesampledperchWecollectedthesamehabitatmeasurementsasthosenotedaboveatthreeheights0515and2mabovethegroundre-sultinginasetofthreerandomperchesforeveryutilizedperchForpercheslt2minheightwesampledonlyat05and15mWallperches
greaterthan50cmindiameterwererecordedas100cmasdiametercannotbesensiblycalculatedforcompletely flatperches (egwalls)andperchesofthissizearelikelyfunctionallyequivalentforsmallliz-ards(egCartmill1985)Welog-transformedperchheightdiameteranddistancetonearestperchesbeforesubsequentstatisticalanalyses
Weanalyzeddifferences inhabitat choiceandniche spacewiththreemainanalysesWeperformedallstatisticalanalysesusingR322(RCoreTeam2015)Firstwetestedfordifferencesinhabitatutilizedbyeachspeciescomparedtotherandomlyavailablehabitat(iehab-itatchoice)byfittingatwo-wayMANOVAforeachspecieswithsiteandsamplenumber(toaccountforcorrelationbetweenavailablehab-itatsamples)ascovariates(residualsforthesemodelscanbefoundinthesupplementalmaterialsS1-S3)WeusedFisherrsquosExactandChi-square tests (as appropriate) to compare perch type used betweenspecies and between each species and randomly available perchesWedidnotincludeperchheightinthisanalysisaswedidnotrandomlysample available perches at the full range of potential heights (egaboveourreach)Secondwedeterminedkeyhabitatvariablesdistin-guishingperchoccupancybetweenthetwospeciesusingconditionalinferenceclassificationtreeanalysisThisanalysisdeterminespredic-tivevariableswiththegreatestexplanatorypowertoseparategroupsandprovidesthresholdestimatesforeachvariableWefitourclassifi-cationmodelusingtheRpackageldquopartyrdquo(HothornHornikampZeileis2006)Finallyweanalyzedhowthetwospeciespartitionthehabitatasawholewithavarimax-rotatedprincipalcomponentanalysisonthecorrelationmatrixforutilizedandavailablehabitatdatausingthevari-ables forwhichhabitatchoicewassuggestedbytheMANOVAsforat leastone speciesWe retainedcomponentswitheigenvaluesgt1
F IGURE 2emsp (a)LocationsofsitessampledInsetinArecibothreelocationsweresurveyed(indicatedbystars)(1)UniversityIneteramericanaArecibo(2)aresidentialneighborhoodand(3)UniversityofPuertoRicoAreciboDashedlinesindicatemajorhighways(thickdash)andmajorsurfaceroads(smalldash)(b)Distributionofhourssampledacrossallsites
Mayaguumlez
San Juan
AguadillaArecibo
0
1
2
3
4
5
8 9 10 11 12 13 14 15 16 17 18 19Time of day
Cou
nt
SiteAguadillaAreciboMayaguezSan JuanU InteramericanaUPR Arecibo
3
2
1
2 Kilometers
0 125 25 50 km
(a) (b)
emspensp emsp | emsp29WINCHELL Et aL
ForretainedcomponentswethencomparedmultidimensionalhabitatusebetweenspecieswithttestsandbetweenutilizedandavailablehabitatwithANOVAandTukeyrsquosHSDposthoctests
3emsp |emspRESULTS
Collectivelywespentatotalof64person-hoursat5urbansitesandrecorded487lizardsOfthese442wereA cristatellus(mean668liz-ards per person-hour per site) and45wereA stratulus (mean073lizardsperperson-hourpersite) Inadditionwesampled31 lizards(n = 20 A cristatellusandn = 11 A stratulus)fromasixthsite(AreciboUI)inwhichwedidnotrecordtotalsightingsOfthese518animalswe sampled a total of 47A stratulus and 52A cristatellus as focalanimalsforhabitatuseandtookatotalof274measuresofpotentialperchsites(ldquoavailablehabitatrdquo)
AssumingdetectionprobabilityissimilarforthetwospeciesA cri-statellusweresignificantlymoreabundantthanA stratulusacrosssites(FisherrsquosExactplt001Figure3a)ComparingallobservedanimalsfromthefivesitesinwhichwerecordedtotalsightingswefoundthatA cristatellus utilizedmanmade substrates such aswalls and fencesat a much higher rate (62) than A stratulus (4) (Fisherrsquos Exactplt001Figure3b)Howeverwhencomparingtheseobservationstoallrandomperchsites(n=96)wefoundthatA stratulususesnaturalsubstratesmorefrequentlythanencountered(FisherrsquosExactplt001)while A cristatellususesmanmadesubstratesatarelativefrequencysimilartotheiravailabilityintheenvironment(χ2p=535)
WefoundthatavailablehabitatdifferedsignificantlyfromutilizedhabitatforA cristatellusinfivevariablesambienttemperaturehumid-ityperchdiameterperchproximityandvegetativecanopycoverInA stratulusavailableandutilizedhabitatdifferedforsevenvariablesambienttemperatureperchtemperatureperchdiametervegetativecanopymanmadecanopyperchtypeandperchroughness(Tables1ndash2Figure4)
In terms of structural habitat (Table2 Figure4) A cristatellus perched lower than A stratulus (mean perch height A cristatellus 1080mmeanperchheightA stratulus1561mt=minus3293df=88p=001) Both species utilized thinner perches than are randomlyavailablewhich isunsurprisinggiventhe largenumberofextremelybroaddiameterperches inurbanareas (egwalls)Anolis cristatellus also chose perches that were less isolated (ie perches that werecloser toanalternateperchsite)whileA stratulusdidnotdiscrimi-nateonthisaxisInadditionA cristatellusdidnotdiscriminatelyusehabitatbasedonperchtype(manmadevsnatural)orsubstraterough-nesswhereasA stratulususednaturalperchesandperchesthathadroughersurfacesatahigherfrequencythanexpectedbasedontheiravailability
Intermsofmicroclimate(Table2Figure4)bothspeciesactivelyselectedmicrohabitatbasedonambienttemperaturethoughinoppo-sitedirectionsA cristatellusutilizedwarmerhabitatwhileA stratulus utilizedcoolerhabitatInadditionA cristatellususedperchesthathadlowerhumidityandA stratulususedperchesthathadlowersurfacetemperaturesAlthoughbothmanmade(shadecastbybuiltstructures)andvegetative(shadecastbytreesorothervegetation)canopycovers
F IGURE 3emsp (a)RelativeabundancesdiffereddramaticallyweencounteredmanymoreA cristatellusacrossallsites(b)AnoliscristatellususedartificialperchesatahigherfrequencythannaturalperchesandatasimilarratetowhatwasavailableAnolis stratulususednaturalperchesalmostexclusively(FisherrsquosExacttestplt001)
0
25
50
75
100
Aguadilla
Arecibo (res)
Arecibo (UPR)
Mayaguez
San Juan
Spe
cies
per
site
(
)
A cristatellusA stratulus
n = 85 n = 251 n = 18 n = 64 n = 54
0
25
50
75
100
A cristatellus
(use)
A stratulus(use)
Available
Per
ch u
se fr
eque
ncy
n = 442 n = 45 n = 96
Perch type
Manmade Natural
(a) (b)
30emsp |emsp emspensp WINCHELL Et aL
werelowacrossallsitesA stratulusdiscriminatelyutilizedperchsiteswithveryhighvegetativecanopycoverandverylowmanmadecovercompared to random perchesAnolis cristatellus also chose percheswithslightlyhighervegetativecanopythanexpectedbychancebutthiseffectwasrelativelyweakandA cristatellusdidnotappeartodis-criminatefororagainstmanmadecover
Wenextanalyzedspeciespresenceataperchsiteusingclassifi-cationtreeanalysistoidentifyhabitatfactorsthatdifferentiateperchappropriateness between the two species (Figure5) This analysis
revealed that habitat use inA stratulus andA cristatellus separatesbasedontwokeyvariablesThespeciesdifferedprimarily inhabitatusebasedonvegetativecanopycover(plt001)withthemajorityofA stratulususingperchescoveredbygreaterthan740treecoverand secondarily based on ambient temperature (p=009) with themajorityofA cristatellus usinghabitatwith lower canopycoverandambienttemperaturesgreaterthan293degC
Lastlyweanalyzedmulti-dimensionalnichespacewithavarimax-rotatedprincipal component analysis of thesehabitatvariablesWeincludedperchheightandsevenoftheeightsignificantvariablesfromtheMANOVAanalyses in thisanalysis todeterminedifferencesbe-tweenspecies inmultivariatenichespaceWe includedonlyoneofthecanopycovervariables(vegetativecanopy)becauseweareinter-estedindescribingnichespacewithoutanyexplicitlyurbanvariablesincluded (egmanmadecanopycover)Principalcomponents1and2were significantly different betweenA stratulus andA cristatellus (t test Table3 Figure6) and the first three principal componentscaptured653ofvarianceVarimax-rotatedcomponent1hadhighpositiveloadingsforambientandperch(surface)temperaturesandahighnegativeloadingforhumidityComponent2hadhighapositiveloadingforperchdiameterandhighnegativeloadingsforvegetativecanopy cover and perch roughness Finally component 3 had highnegativeloadingsforperchheightandproximitytonearestperch
Weanticipated thatmanyof the relevantenvironmental factorscould be associatedwith artificial substrates sowe also comparedmultidimensionalnichespaceofavailableandutilizedperchesassoci-atedwithnaturalandartificialsubstrates(Figure7)Availablehabitatdifferedbetweenartificialandnaturalperchtypesforallthreeprin-cipalcomponentssuggestingthathabitatassociatedwithmanmadeperchesdiffersfromthatassociatedwithnaturalperchesinmultipledimensions (Figure7Table3) Finallywe compared utilized habitatseparatedbyperchtypeforA cristatellustoutilizedhabitatforA strat-ulusWefoundthatmanmadeperchesusedbyA cristatellusdifferedfromnaturalperchesusedbyA cristatellusandfromallperchesusedbyA stratulusforPC1andPC2(Figure7Table4)suggestingthatdi-vergenceinhabitatusebetweenthespeciesisassociatedwiththeuseofmanmadeperches
4emsp |emspDISCUSSION
41emsp|emspAbundance
We found that A cristatellus was significantly more abundant thanA stratulusatsampledurbansitesInparticularweencounterednearly10timesasmanyA cristatellusasA stratulusacrossallsitesandtheformer specieswas encountered at amuch higher rate per person-hour This finding could simply be a consequence of differences inabundanceinnaturalhabitatsnearbyBothA cristatellusandA stratu-lusarelocallyabundantinnaturalhabitatsinPuertoRicowithsympat-ricdensitiesinmesichabitatsatgroundlevelestimatedat1000ndash1100and 600ndash900 per hectare respectively (Rodda Perry Rondeau ampLazell 2001) If fewerA stratulus are found innearbynatural areasthenwemightexpecturbanhabitatstoinheritthisnaturaldifference
TABLE 1emspResultsfromMANOVAsforhabitatuseversusavailabilityfortheninehabitatvariablescomparingthesixurbansitesandhabitatchoiceDegreesoffreedom(df)Fandp-value(p)aregivenforeach
Wilksrsquo lambda df F p
Anolis cristatellus
Habitatchoice 0569 1216 17459 lt001
Urbansite 0025 5216 26549 lt001
Anolis stratulus
Habitatchoice 0247 1212 68827 lt001
Urbansite 0010 5212 36574 lt001
Statistically significant values forhabitat choice areboldedand indicatedifferencesbetweenutilizedandrandomlyavailablehabitat
TABLE 2emspResultsfromANCOVAsforhabitatchoicesubsequenttotheMANOVAsinTable1Degreesoffreedom(df)Fandp-value(p)aregivenforeach
df F p
Anolis cristatellus
Ambienttemperature 1216 55822 lt001
Perchtemperature 1216 0331 566
Humidity 1216 99237 lt001
Perchheight 1216 5868 016
Perchdiameter 1216 9012 003
Perchproximity 1216 23067 lt001
Vegetativecanopy 1216 4028 046
Manmadecanopy 1216 1437 232
Perchroughness 1216 1589 209
Anolis stratulus
Ambienttemperature 1212 47060 lt001
Perchtemperature 1212 29113 lt001
Humidity 1212 2660 104
Perchheight 1212 0197 658
Perchdiameter 1212 40113 lt001
Perchproximity 1212 0187 666
Vegetativecanopy 1212 319157 lt001
Manmadecanopy 1212 104938 lt001
Perchroughness 1212 238820 lt001
Shadedcellsaresignificantfordifferencebetweenuseandavailabilityatthesignificancelevelindicatedbythelastcolumn
emspensp emsp | emsp31WINCHELL Et aL
inabundancebetweenspeciesHoweverthedifferenceinabundancesmeasured inthepresentstudyfarexceedsthatfoundpreviouslyforPuertoRicanmesicforest(egRoddaetal2001)ThissuggeststhaturbanhabitatsdonotsupportA stratulusandA cristatellusinrelativeabundances proportional to those reported for more natural sitesRelative abundances in urban areas instead appear to follow a pat-ternmorecloselyresemblingnaturallyxericforests(egGenetGenetBurtonampMurphy2001)despitebeinglocatedinmesicregions
ItispossiblethatoursamplingmethodmayhavefailedtodetectA stratulus perching higher in the urban canopy Indeed in naturalhabitatsA stratulus densityhasbeenunderestimatedat somesiteswhentheyutilizecanopyhabitatForexampleReagan(1992)found
thatA stratulusattainsextremelyhighdensities(24000ndash28000ha)inforestswhereindividualsoccupyhighcanopyhabitat(approximately10ndash20mheight)Webelievethisisnotamajorconcerninourstudyasurbantreesatoursitestendedtobeshorterandrarelyproduced
F IGURE 4emspMeanandSEforhabitatvariablessampledforhabitatavailability(ldquoArdquo)andeachspeciesuse(ldquoCrdquomdashA cristatellusldquoSrdquomdashA stratulus)Differencesbetweenutilizedandavailablehabitat(summarizedinTable2)representedbygraylinesandsignificancelevelplt001plt01plt05
Ambient temp (degC)
295
300
305
310
Manmade canopy ()
10
20
Perch height (cm)
44
46
48
50
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
Perch diameter (cm)
24
27
30
33
Nearest perch (cm)
46
48
50
52
Relative humidity ()
52
54
56
58
60
290
295
300
305
Veg canop y ()
40
50
60
70
80
(log
scal
e)
Surface roughness
35
40
45
Perch temp (degC)
F IGURE 5emspClassificationtreeforhabitatusedifferencesinA cristatellusandA stratulusSpeciespercentagesindicatethepercentageofallsampledindividualsofeachspeciesineachgroup(highcanopycoverlowcanopycoverandhightemperaturelowcanopycoverandlowtemperature)
Veg canopy p lt 0001
le7404 cover gt7404 cover
Ambient tempp = 0009
le293degC gt293degC
A cristatellus 58A stratulus 149
A cristatellus 712A stratulus 8 5
A cristatellus 231A stratulus 766
TABLE 3emspResultsfromvarimax-rotatedprinciplecomponentanalysisofurbanhabitat
PC1 PC2 PC3
Humidity minus0560 0118 minus0163
Ambienttemp 0616 minus0008 0010
Perchheight minus0112 minus0040 minus0571
Perchdiameter minus0188 0477 minus0048
Nearestperch 0136 0011 minus0786
Vegcanopy minus0125 minus0631 0014
Perchtemp 0473 0108 minus0136
Perchroughness minus0042 minus0589 minus0087
Cumulativevariance 2687 5205 6528
SignificanceSpecies plt001 p = 001 p = 107
Significanceperchtype plt001 plt001 p = 002
Eigenvalue 2150 2015 1058
SignificanceforttestscomparingprincipalcomponentsbetweenA stratu-lusandA cristatellusaregivenintherowlabelledldquoSignificanceSpeciesrdquoandsignificanceforttestscomparingprincipalcomponentsbetweennatu-ralandmanmadeperchesaregivenintherowlabelledldquoSignificancePerchTyperdquoSignificantloadingsareboldedandshadedSignificancelevelsforspeciesandperchtypeANOVAsareplt001plt01
32emsp |emsp emspensp WINCHELL Et aL
dense or continuous canopy Moreover manmade substrates suchaswallsandfencesareclearlyvisibleall thewaytotherooflineAssuchvisibilityofthefewhighperchespresentwasverygoodacrossallurbansitesandwedonotexpectthatwefailedtoobserveasignif-icantnumberofindividualsathigherperches
42emsp|emspHabitat use
ThetwolizardspeciesofthisstudydifferedinthefrequencywhichtheyutilizedmanmadesubstratesasperchesAnolis cristatellususedman-madeperchesatahighfrequencybutusedbothmanmadestructuresandvegetationinproportiontotheirrelativeabundanceintheenviron-mentIncontrastA stratulusinfrequentlyoccupiedmanmadeperchesSimilarlyKolbeBattlesandAvileacutes-Rodriacuteguez(2015)foundthatA cris-tatellususedmanmadestructuresmorefrequentlythanA stratulus in human-modifiedhabitatsdespitefindingA stratulustobemoreadeptatsprintingonsmoothverticalsurfacesOurdatasuggestthatA stratu-luseitheractivelyseeksoutnaturalsubstratesoravoidstheuseofman-madesubstratesThispatternmaybeexplainedbysomecombinationofpredationcompetitionperformanceandhabitatrequirements
AtfirstglanceitappearsthatA cristatellusandA stratuluspartitionurbanniche space in similarwaysas innatural foresthabitatWhenfoundsyntopicallyinnaturalforesthabitatthesetwospeciesdividethehabitatsuchasmanyanolespeciesbasedprimarilyonstructuralandmicroclimatichabitatfeatures(Rand1964reviewedinLosos2009)InnaturalhabitatsA cristatellustypicallyusesbroaderandlowerpercheswhile A stratulususesthinnerandhigherperches(Cooper2005Rand
F IGURE 6emspPrincipalcomponents12and3plottedwith95confidenceintervalellipsesforutilizedhabitatbyeachspeciesPC1andPC2differedbetweenspeciesatsignificancelevelsplt001()andplt01()respectively
minus25
00
25
minus25 00 25 minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
A cristatellus
A stratulus
PC3
A cristatellus
A stratulus Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower perchesLess isolated perches
F IGURE 7emspPrincipalcomponents1and2plottedwith95confidenceintervalellipsesgroupedbyperchtypeforavailablehabitat(left)andutilizedhabitat(right)
Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower humidityHigher temperature (ambient amp perch)
A cristatellusManmade perches
A cristatellusNatural perches
A stratulusminus25
00
25
minus25 00 25
PC1
minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
Natural perches
Manmadeperches
TABLE 4emspResultsofANOVAandTukeyrsquosHSDcomparingprincipalcomponentsbetweenutilizedhabitatbyA stratulus(all)andA cristatellus(byperchtype)Degreesoffreedom(df)Fandp-value(p)aregivenforeachtest
ANOVA Tukeyrsquos HSD
df F p CNndashCM CNndashS CMndashS
PC1 286 24970 lt001 0313 001 lt001
PC2 286 28890 lt001 lt001 695 lt001
PC3 286 1323 272 1000 413 361
PairedcomparisonsfortheTukeyrsquosHSDtestsareA cristatellususingnatu-ralperchesversusA cristatellususingmanmadeperches(CNndashCM)A cris-tatellususingnaturalperchesversusA stratulusonallperches(CNndashS)andA cristatellus using manmade perches versus A stratulus on all perches(CMndashS)Significancelevelsplt001plt01plt05Significantre-sultsareboldedandshaded
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
26emsp |emsp emspensp WINCHELL Et aL
Amajor consequence of urbanization is the filtering of speciesoften resulting in lower biodiversity such that a subset of the orig-inal native community is represented in theurbanhabitat (Aronsonetal2014Forman2014)Ingeneralurbancommunitiesaredomi-natedbyurban-tolerantspecieswithabundancesdecliningasurban-izationincreasesanddiversitydecliningascitiesage(Forman2014GrantMiddendorfColganAhmadampVogel2011McKinney2008ShochatWarrenFaethMcIntyreampHope2006)Howeverurbaniza-tioncangeneratenovelhabitatspaceundersomecircumstancesre-sultinginnewecologicalopportunitiesandspeciescolonizationWhilethismay leadtoenhancedabundanceanddiversity theseadditionstypicallyconsistofnonnativespecies(McKinney2002Shochatetal2006)Nonethelessurbanareascanstillsupportsubstantialbiodiver-sity(Forman2014)
Some species are able to adapt to changes associatedwith ur-banization (eg Harris Munshi-South Obergfell amp OrsquoNeill 2013Winchell Reynolds Prado-Irwin Puente-Roloacuten amp Revell 2016)Speciesthatpersistinurbanhabitatstendtohaveseveralcharacteris-ticsincommonbroadhabitatanddietrequirements(generalists)highmobilitylargereproductiveoutputsmallbodysizeandtoleranceofhumandisturbances(Grantetal2011)Yetdifferencesintolerancesandpreferencesbetweenspeciesmeanthatnotallspeciesareabletosimilarlymeettheirneedsinurbanenvironments
Animalsthatpersistinurbanareasfaceamodifiedhabitatdom-inated by human structures lacking continuous canopy cover andexhibitingdifferentthermalandhydrologicconditionsfromthoseofnaturalareasnearby(reviewedinForman2014)Somespeciespersistinurbanareasbutarestilldependentonnearbynaturalareastomain-tainpositivepopulationgrowthSuchspeciesareoftenreferredtoasldquotolerantrdquo or ldquourban adaptersrdquo (McKinney 2002) By contrast otherspeciesfoundinurbanhabitatshavefullyembracedtheirnewfoundmilieu utilize anthropogenic resources extensively and may evenachievehigherpopulationgrowthratesanddensities inurbanareasthanatnaturalsitesThesespeciesarereferredtoasldquosynanthropicrdquoldquourbanophilicrdquoorldquourbanexploitersrdquo(Forman2014Grantetal2011McKinney2006)
For urbanophiles urbanization may have created a preferablehabitatwhencomparedtotheirhistoricnaturalareawithabundantfoodrefugesandaccesstomatesForexampleanthropogenicwastealongwithinsectsattractedtothiswasteandtoartificiallightsourcesmayincreasetheavailabilityoffoodonlocalscalesforinsectivorousherpetofauna (Henderson amp Powell 2001 Perry Buchanan FisherSalmonampWise2008)Shochatetal(2010)foundthatelevatedden-sitiesofsomeurbanbirdspeciescanbeattributedtobothbottom-up(more food resources) and top-down (relaxed predation) controlsUrbanophilicspeciesnotonlypersist inurbanhabitatsbutalsotakefulladvantageofthenovelenvironmentanditsresourceseffectivelyexpandingintothenewnichespacethatcanbeassociatedwithman-madestructuresandresources
Puerto Rico provides an excellent opportunity to study animalresponses to long-term and intensifying human-modification of theenvironment Human settlement of the island by indigenous peo-ples began 5000years before the present day andwas succeeded
by intensive European settlement beginning in the early 16th cen-turyTheseerasof colonizationhave resulted in successiveperiodsof intensehabitatmodification InparticularPuertoRicowasnearlycompletelydeforestedforthepurposesofagricultureThisperiodofdeforestationpeakedinthe1940swhenaslittleas6forestcoverremainedontheisland(Koenig1953MillerampLugo2009)Overthepastsevendecadesforestcoverhasprogressivelyregeneratedasag-ricultural lifestyleswere abandoned and industrialization increasedbut this has been concurrentwith an expansion and intensificationof urban development island-wide (Martinuzzi Gould amp RamosGonzaacutelez2007MillerampLugo2009)Thenetresultofthisdeclineinagriculturalandincreaseinindustrializationhasbeenadramaticriseintheextentofurbanareasbyanestimated42infewerthantwodecades(Helmer2004LoacutepezAideampThomlinson2001)
Presentlyurbanareascover11oftheislandandcontinuetointensifyinspatialextentandpopulationdensity(Martinuzzietal2007MillerampLugo2009USCensusBureau2012)Urbanareasarecharacterizedbylargepercentagesofimpervioussurfaces(egroadsconcrete)andlowlevelsofvegetativecanopycoverWithapopulationof3725789(938ofwhichresideinurbanareasUSCensusBureau2012)PuertoRicorsquosurbanareasincludelow-densityurbanization (suchas ruralcommunities)midsizecitiesdominatedby suburban communities and sprawlingmetropolitan areaswithlittle tono remainingnaturalhabitat andmore thanamillion res-idents(egMetropolitanSanJuan)This intenselandmodificationand the pressures associatedwith human presence have resultedinadeclineofmanynativeplantandanimalspecies(Koenig1953MillerampLugo2009)Despitethiscenturies-longprocessofurban-ization many native Puerto Rican species persist in and aroundurbansites
ThePuertoRicanCrestedAnoleAnolis cristatellusandtheBarredAnoleAnolis stratulus(Figure1)areperhapsthemostcommonurbananolespeciesinPuertoRicoandaretheonlytwowehaveregularlyobservedinvirtuallyalltypesofurbanareasisland-wideBothspeciesare relatively small arboreal lizards (adultmale SVL 50ndash75mm and35ndash55mm respectively)Anoles are characterized by the repeatedindependentevolutionofecologicallyandmorphologicallysimilarmi-crohabitatspecialists(ldquoecomorphsrdquo)ondifferentislandsAmongtheseAnolis cristatellusiscategorizedasaldquotrunk-groundrdquospecialistwhereasA stratulusisaldquotrunk-crownrdquospecialist(Losos2009)Thesedesigna-tionsaredefinedbybothhabitatuseandmorphologyTrunk-groundanolessuchasA cristatellusarebrownincolorhaverelativelylonglimbsastockybuildandperchlowtothegroundonbroadsurfacessuchastreetrunksIncontrasttrunk-crownanolessuchasA stratu-lusaretypicallygreenincolor(althoughA stratulusislightgray)haverelativelyshort limbsaremoreslenderandperchfromeye-level tohighupintreesutilizingleavestwigsbranchesandtrunksasperches(reviewedinLosos2009)
Anolis cristatellusandA stratulusarefoundatlowerelevationsandinbothmesicandxerichabitatswheretheyexperiencehighertem-peratureandlowerhumiditycomparedtomanyuplandspecieswithmorestrictthermalrequirements(Rand1964)Thusitisperhapsun-surprisingthatbothspeciesaretolerantofurbanhabitatwhichtends
emspensp emsp | emsp27WINCHELL Et aL
to be warmer and drier than nearby forests (reviewed in Forman2014)Wherethetwospeciesco-occurinnaturalforesthabitatstheypartitionthehabitatstructurallyandclimaticallySpecificallypriorre-search suggests thatA stratulus utilizeshigher and thinnerperchesandperchsitesthatarecoolerhigherinhumidityandhavemoreex-tensivecanopycovercomparedtohabitatusedbyA cristatellus(Rand1964Reagan1992)
Hereweaskhowthesetwospeciesutilizeandpartitionanovelhabitat urban areas Our null hypothesis is that theywill maintainniche partitioning and habitat choices in the samemanner as theydointhenaturalforesthabitatschoosingnaturalsubstratesthatfittheirpreferencesInotherwordsA stratuluswillseekouthigherthin-nercoolerpercheswiththickercanopycoverwhileA cristatellus will seekoutlowerbroaderwarmerpercheswiththinnercanopycoverAlternativelybothspeciesmayutilize thenovelnichespaceassoci-atedwithmanmadehabitat(ieonandaroundbuildings)Athirdpos-sibilityisthatonlyonespeciesexpandsintothenovelhabitatspaceassociated with anthropogenic resources while the other remainsstrictlyassociatedwithnaturalaspectsoftheurbanspace
WetestedthesehypothesesbymeasuringtherelativeabundancehabitatuseandnichespaceoccupiedbythesetwospeciesinurbanareasBecauseA cristatellus ismoreofageneralistwepredict thatitwilloccupyagreaterportionoftheurbanhabitatspaceandmoreextensively utilize habitat associatedwith anthropogenic structureswhile A stratuluswillremainassociatedwithnaturalhabitatelementsSimilartonaturalhabitatswealsopredictthateachspecieswillnon-randomlyutilizeperchesthatbestmeettheirstructuralandclimaticpreferencesasobserved innatural areasUnderstandingdifferentialhabitatuseinurbanpersistentspeciesshedslightonthefactorsinflu-encingurbantolerance(thegeneralcapacitytopersistinurbanareas)versusgenuineurbanophilyHereweprovideanempiricaltestofthisecological theoryMoreover this typeofnaturalhistory informationcanaidconservationinurbanareasbyidentifyingtheminimumhab-itat requirementsofnative species and thepotential forurbanper-sistenceandadaptation
2emsp |emspMATERIALS AND METHODS
From24April2015to6May2015wesampledsixurbansitesinfourmunicipalitiesinnorthernandwesternPuertoRicoSanJuanAreciboAguadilla and Mayaguumlez (Figure2a) In San Juan Aguadilla andMayaguumlez thesiteswereresidentialneighborhoods InArecibowesampledoneresidentialneighborhoodandtwouniversitycampuses(UniversityofPuertoRicoAreciboandUniversityInteramericana)ForlogisticalreasonswedidnotsamplenearbyforestedareasOurvisualsamplingmethodsusedintheurbanhabitatwouldlikelyhavebeenin-adequateinforesthabitatsduetothedifferencesinstructuralhabitatcomplexityandcanopyusebyA stratulus
Ateachlocalitywesampledabundancebyslowlywalkingthroughthehabitatforaminimumof3hrwithoutretracingourpathbetween8amand7pm(dusk)Becausethesespeciesvaryintheirhabitatusethroughoutthedayinnaturalforesthabitats(Hertz1992Nicholsonetal2005)andinurbanhabitats(Avileacutes-Rodriacuteguezunpublished data)surveyswereconductedatdifferenttimesofthedaywithatleastonesite surveyedduring each daylight hour (Figure2b) For every adultlizardobservedwerecordedspeciesandperchsubstrate
Wechosea subsetof theobserved lizardsas focalanimalsWeonlychosefocalanimalsoccupyinguniqueperchestoavoidaccidentalpseudoreplication(iewedidnotsamplemultiplelizardsofthesame
F IGURE 1emspAnolis cristatellus(topphotoEJC)andAnolis stratulus (bottomphotoKMW)occupydifferentportionsoftheurbanhabitat
(a)
(b)
28emsp |emsp emspensp WINCHELL Et aL
speciesutilizingthesametree)BecauseofdifferencesinabundancewesampledeveryA stratulusoccupyingauniqueperchandthenextobservedA cristatellus resulting inapproximatelyequalnumbersoffocalobservationsperspeciesForfocalanimalswenotedenviron-mentalconditionsandhabitatuseambienttemperature(digitalprobeOMEGAHH12B)perchtemperature(infraredprobeEXTECHIR201)relativehumidity(digitalmeterAMPROBETHWD-3)sunconditionsperchheightperchdiameterdistancetonearestpotentialperch(anystructureatleast05mhighandrobustenoughtosupporttheweightofanadultofeitherspecies)perchtypeandperchroughnessPerchroughnesswasratedonascaleof1ndash5withlowernumbersindicatingsmoothersubstratesRatingswereasfollows(basedonpreviousanal-ysesofsurfaceroughnessandsubstratetypeWinchelletal2016)(1)glass(2)metal(3)paintedconcrete(4)unpaintedprocessedwoodleaves and smooth bark trees such as bamboo and (5) thick barktreessuchasTababuya amarilloandCalophyllum antillanumaswellasunpainted andweathered concreteWe took photos of the canopyimmediatelyabovetheperchsite(OlympusEP5withOlympus9mm180fisheye)Weestimatedvegetativecanopycoverandmanmadecanopycover(iemanmadestructuresobscuringthesky)fromthesephotographsusingAdobePhotoshop(CS51)
Foreveryfocalanimalwealsosampledavailablehabitatbyran-domlyselectinganearbyperchWesamplednearbyavailableperchesbychoosingtheclosestpotentialperchinarandomdirectionfromthesampledperchWecollectedthesamehabitatmeasurementsasthosenotedaboveatthreeheights0515and2mabovethegroundre-sultinginasetofthreerandomperchesforeveryutilizedperchForpercheslt2minheightwesampledonlyat05and15mWallperches
greaterthan50cmindiameterwererecordedas100cmasdiametercannotbesensiblycalculatedforcompletely flatperches (egwalls)andperchesofthissizearelikelyfunctionallyequivalentforsmallliz-ards(egCartmill1985)Welog-transformedperchheightdiameteranddistancetonearestperchesbeforesubsequentstatisticalanalyses
Weanalyzeddifferences inhabitat choiceandniche spacewiththreemainanalysesWeperformedallstatisticalanalysesusingR322(RCoreTeam2015)Firstwetestedfordifferencesinhabitatutilizedbyeachspeciescomparedtotherandomlyavailablehabitat(iehab-itatchoice)byfittingatwo-wayMANOVAforeachspecieswithsiteandsamplenumber(toaccountforcorrelationbetweenavailablehab-itatsamples)ascovariates(residualsforthesemodelscanbefoundinthesupplementalmaterialsS1-S3)WeusedFisherrsquosExactandChi-square tests (as appropriate) to compare perch type used betweenspecies and between each species and randomly available perchesWedidnotincludeperchheightinthisanalysisaswedidnotrandomlysample available perches at the full range of potential heights (egaboveourreach)Secondwedeterminedkeyhabitatvariablesdistin-guishingperchoccupancybetweenthetwospeciesusingconditionalinferenceclassificationtreeanalysisThisanalysisdeterminespredic-tivevariableswiththegreatestexplanatorypowertoseparategroupsandprovidesthresholdestimatesforeachvariableWefitourclassifi-cationmodelusingtheRpackageldquopartyrdquo(HothornHornikampZeileis2006)Finallyweanalyzedhowthetwospeciespartitionthehabitatasawholewithavarimax-rotatedprincipalcomponentanalysisonthecorrelationmatrixforutilizedandavailablehabitatdatausingthevari-ables forwhichhabitatchoicewassuggestedbytheMANOVAsforat leastone speciesWe retainedcomponentswitheigenvaluesgt1
F IGURE 2emsp (a)LocationsofsitessampledInsetinArecibothreelocationsweresurveyed(indicatedbystars)(1)UniversityIneteramericanaArecibo(2)aresidentialneighborhoodand(3)UniversityofPuertoRicoAreciboDashedlinesindicatemajorhighways(thickdash)andmajorsurfaceroads(smalldash)(b)Distributionofhourssampledacrossallsites
Mayaguumlez
San Juan
AguadillaArecibo
0
1
2
3
4
5
8 9 10 11 12 13 14 15 16 17 18 19Time of day
Cou
nt
SiteAguadillaAreciboMayaguezSan JuanU InteramericanaUPR Arecibo
3
2
1
2 Kilometers
0 125 25 50 km
(a) (b)
emspensp emsp | emsp29WINCHELL Et aL
ForretainedcomponentswethencomparedmultidimensionalhabitatusebetweenspecieswithttestsandbetweenutilizedandavailablehabitatwithANOVAandTukeyrsquosHSDposthoctests
3emsp |emspRESULTS
Collectivelywespentatotalof64person-hoursat5urbansitesandrecorded487lizardsOfthese442wereA cristatellus(mean668liz-ards per person-hour per site) and45wereA stratulus (mean073lizardsperperson-hourpersite) Inadditionwesampled31 lizards(n = 20 A cristatellusandn = 11 A stratulus)fromasixthsite(AreciboUI)inwhichwedidnotrecordtotalsightingsOfthese518animalswe sampled a total of 47A stratulus and 52A cristatellus as focalanimalsforhabitatuseandtookatotalof274measuresofpotentialperchsites(ldquoavailablehabitatrdquo)
AssumingdetectionprobabilityissimilarforthetwospeciesA cri-statellusweresignificantlymoreabundantthanA stratulusacrosssites(FisherrsquosExactplt001Figure3a)ComparingallobservedanimalsfromthefivesitesinwhichwerecordedtotalsightingswefoundthatA cristatellus utilizedmanmade substrates such aswalls and fencesat a much higher rate (62) than A stratulus (4) (Fisherrsquos Exactplt001Figure3b)Howeverwhencomparingtheseobservationstoallrandomperchsites(n=96)wefoundthatA stratulususesnaturalsubstratesmorefrequentlythanencountered(FisherrsquosExactplt001)while A cristatellususesmanmadesubstratesatarelativefrequencysimilartotheiravailabilityintheenvironment(χ2p=535)
WefoundthatavailablehabitatdifferedsignificantlyfromutilizedhabitatforA cristatellusinfivevariablesambienttemperaturehumid-ityperchdiameterperchproximityandvegetativecanopycoverInA stratulusavailableandutilizedhabitatdifferedforsevenvariablesambienttemperatureperchtemperatureperchdiametervegetativecanopymanmadecanopyperchtypeandperchroughness(Tables1ndash2Figure4)
In terms of structural habitat (Table2 Figure4) A cristatellus perched lower than A stratulus (mean perch height A cristatellus 1080mmeanperchheightA stratulus1561mt=minus3293df=88p=001) Both species utilized thinner perches than are randomlyavailablewhich isunsurprisinggiventhe largenumberofextremelybroaddiameterperches inurbanareas (egwalls)Anolis cristatellus also chose perches that were less isolated (ie perches that werecloser toanalternateperchsite)whileA stratulusdidnotdiscrimi-nateonthisaxisInadditionA cristatellusdidnotdiscriminatelyusehabitatbasedonperchtype(manmadevsnatural)orsubstraterough-nesswhereasA stratulususednaturalperchesandperchesthathadroughersurfacesatahigherfrequencythanexpectedbasedontheiravailability
Intermsofmicroclimate(Table2Figure4)bothspeciesactivelyselectedmicrohabitatbasedonambienttemperaturethoughinoppo-sitedirectionsA cristatellusutilizedwarmerhabitatwhileA stratulus utilizedcoolerhabitatInadditionA cristatellususedperchesthathadlowerhumidityandA stratulususedperchesthathadlowersurfacetemperaturesAlthoughbothmanmade(shadecastbybuiltstructures)andvegetative(shadecastbytreesorothervegetation)canopycovers
F IGURE 3emsp (a)RelativeabundancesdiffereddramaticallyweencounteredmanymoreA cristatellusacrossallsites(b)AnoliscristatellususedartificialperchesatahigherfrequencythannaturalperchesandatasimilarratetowhatwasavailableAnolis stratulususednaturalperchesalmostexclusively(FisherrsquosExacttestplt001)
0
25
50
75
100
Aguadilla
Arecibo (res)
Arecibo (UPR)
Mayaguez
San Juan
Spe
cies
per
site
(
)
A cristatellusA stratulus
n = 85 n = 251 n = 18 n = 64 n = 54
0
25
50
75
100
A cristatellus
(use)
A stratulus(use)
Available
Per
ch u
se fr
eque
ncy
n = 442 n = 45 n = 96
Perch type
Manmade Natural
(a) (b)
30emsp |emsp emspensp WINCHELL Et aL
werelowacrossallsitesA stratulusdiscriminatelyutilizedperchsiteswithveryhighvegetativecanopycoverandverylowmanmadecovercompared to random perchesAnolis cristatellus also chose percheswithslightlyhighervegetativecanopythanexpectedbychancebutthiseffectwasrelativelyweakandA cristatellusdidnotappeartodis-criminatefororagainstmanmadecover
Wenextanalyzedspeciespresenceataperchsiteusingclassifi-cationtreeanalysistoidentifyhabitatfactorsthatdifferentiateperchappropriateness between the two species (Figure5) This analysis
revealed that habitat use inA stratulus andA cristatellus separatesbasedontwokeyvariablesThespeciesdifferedprimarily inhabitatusebasedonvegetativecanopycover(plt001)withthemajorityofA stratulususingperchescoveredbygreaterthan740treecoverand secondarily based on ambient temperature (p=009) with themajorityofA cristatellus usinghabitatwith lower canopycoverandambienttemperaturesgreaterthan293degC
Lastlyweanalyzedmulti-dimensionalnichespacewithavarimax-rotatedprincipal component analysis of thesehabitatvariablesWeincludedperchheightandsevenoftheeightsignificantvariablesfromtheMANOVAanalyses in thisanalysis todeterminedifferencesbe-tweenspecies inmultivariatenichespaceWe includedonlyoneofthecanopycovervariables(vegetativecanopy)becauseweareinter-estedindescribingnichespacewithoutanyexplicitlyurbanvariablesincluded (egmanmadecanopycover)Principalcomponents1and2were significantly different betweenA stratulus andA cristatellus (t test Table3 Figure6) and the first three principal componentscaptured653ofvarianceVarimax-rotatedcomponent1hadhighpositiveloadingsforambientandperch(surface)temperaturesandahighnegativeloadingforhumidityComponent2hadhighapositiveloadingforperchdiameterandhighnegativeloadingsforvegetativecanopy cover and perch roughness Finally component 3 had highnegativeloadingsforperchheightandproximitytonearestperch
Weanticipated thatmanyof the relevantenvironmental factorscould be associatedwith artificial substrates sowe also comparedmultidimensionalnichespaceofavailableandutilizedperchesassoci-atedwithnaturalandartificialsubstrates(Figure7)Availablehabitatdifferedbetweenartificialandnaturalperchtypesforallthreeprin-cipalcomponentssuggestingthathabitatassociatedwithmanmadeperchesdiffersfromthatassociatedwithnaturalperchesinmultipledimensions (Figure7Table3) Finallywe compared utilized habitatseparatedbyperchtypeforA cristatellustoutilizedhabitatforA strat-ulusWefoundthatmanmadeperchesusedbyA cristatellusdifferedfromnaturalperchesusedbyA cristatellusandfromallperchesusedbyA stratulusforPC1andPC2(Figure7Table4)suggestingthatdi-vergenceinhabitatusebetweenthespeciesisassociatedwiththeuseofmanmadeperches
4emsp |emspDISCUSSION
41emsp|emspAbundance
We found that A cristatellus was significantly more abundant thanA stratulusatsampledurbansitesInparticularweencounterednearly10timesasmanyA cristatellusasA stratulusacrossallsitesandtheformer specieswas encountered at amuch higher rate per person-hour This finding could simply be a consequence of differences inabundanceinnaturalhabitatsnearbyBothA cristatellusandA stratu-lusarelocallyabundantinnaturalhabitatsinPuertoRicowithsympat-ricdensitiesinmesichabitatsatgroundlevelestimatedat1000ndash1100and 600ndash900 per hectare respectively (Rodda Perry Rondeau ampLazell 2001) If fewerA stratulus are found innearbynatural areasthenwemightexpecturbanhabitatstoinheritthisnaturaldifference
TABLE 1emspResultsfromMANOVAsforhabitatuseversusavailabilityfortheninehabitatvariablescomparingthesixurbansitesandhabitatchoiceDegreesoffreedom(df)Fandp-value(p)aregivenforeach
Wilksrsquo lambda df F p
Anolis cristatellus
Habitatchoice 0569 1216 17459 lt001
Urbansite 0025 5216 26549 lt001
Anolis stratulus
Habitatchoice 0247 1212 68827 lt001
Urbansite 0010 5212 36574 lt001
Statistically significant values forhabitat choice areboldedand indicatedifferencesbetweenutilizedandrandomlyavailablehabitat
TABLE 2emspResultsfromANCOVAsforhabitatchoicesubsequenttotheMANOVAsinTable1Degreesoffreedom(df)Fandp-value(p)aregivenforeach
df F p
Anolis cristatellus
Ambienttemperature 1216 55822 lt001
Perchtemperature 1216 0331 566
Humidity 1216 99237 lt001
Perchheight 1216 5868 016
Perchdiameter 1216 9012 003
Perchproximity 1216 23067 lt001
Vegetativecanopy 1216 4028 046
Manmadecanopy 1216 1437 232
Perchroughness 1216 1589 209
Anolis stratulus
Ambienttemperature 1212 47060 lt001
Perchtemperature 1212 29113 lt001
Humidity 1212 2660 104
Perchheight 1212 0197 658
Perchdiameter 1212 40113 lt001
Perchproximity 1212 0187 666
Vegetativecanopy 1212 319157 lt001
Manmadecanopy 1212 104938 lt001
Perchroughness 1212 238820 lt001
Shadedcellsaresignificantfordifferencebetweenuseandavailabilityatthesignificancelevelindicatedbythelastcolumn
emspensp emsp | emsp31WINCHELL Et aL
inabundancebetweenspeciesHoweverthedifferenceinabundancesmeasured inthepresentstudyfarexceedsthatfoundpreviouslyforPuertoRicanmesicforest(egRoddaetal2001)ThissuggeststhaturbanhabitatsdonotsupportA stratulusandA cristatellusinrelativeabundances proportional to those reported for more natural sitesRelative abundances in urban areas instead appear to follow a pat-ternmorecloselyresemblingnaturallyxericforests(egGenetGenetBurtonampMurphy2001)despitebeinglocatedinmesicregions
ItispossiblethatoursamplingmethodmayhavefailedtodetectA stratulus perching higher in the urban canopy Indeed in naturalhabitatsA stratulus densityhasbeenunderestimatedat somesiteswhentheyutilizecanopyhabitatForexampleReagan(1992)found
thatA stratulusattainsextremelyhighdensities(24000ndash28000ha)inforestswhereindividualsoccupyhighcanopyhabitat(approximately10ndash20mheight)Webelievethisisnotamajorconcerninourstudyasurbantreesatoursitestendedtobeshorterandrarelyproduced
F IGURE 4emspMeanandSEforhabitatvariablessampledforhabitatavailability(ldquoArdquo)andeachspeciesuse(ldquoCrdquomdashA cristatellusldquoSrdquomdashA stratulus)Differencesbetweenutilizedandavailablehabitat(summarizedinTable2)representedbygraylinesandsignificancelevelplt001plt01plt05
Ambient temp (degC)
295
300
305
310
Manmade canopy ()
10
20
Perch height (cm)
44
46
48
50
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
Perch diameter (cm)
24
27
30
33
Nearest perch (cm)
46
48
50
52
Relative humidity ()
52
54
56
58
60
290
295
300
305
Veg canop y ()
40
50
60
70
80
(log
scal
e)
Surface roughness
35
40
45
Perch temp (degC)
F IGURE 5emspClassificationtreeforhabitatusedifferencesinA cristatellusandA stratulusSpeciespercentagesindicatethepercentageofallsampledindividualsofeachspeciesineachgroup(highcanopycoverlowcanopycoverandhightemperaturelowcanopycoverandlowtemperature)
Veg canopy p lt 0001
le7404 cover gt7404 cover
Ambient tempp = 0009
le293degC gt293degC
A cristatellus 58A stratulus 149
A cristatellus 712A stratulus 8 5
A cristatellus 231A stratulus 766
TABLE 3emspResultsfromvarimax-rotatedprinciplecomponentanalysisofurbanhabitat
PC1 PC2 PC3
Humidity minus0560 0118 minus0163
Ambienttemp 0616 minus0008 0010
Perchheight minus0112 minus0040 minus0571
Perchdiameter minus0188 0477 minus0048
Nearestperch 0136 0011 minus0786
Vegcanopy minus0125 minus0631 0014
Perchtemp 0473 0108 minus0136
Perchroughness minus0042 minus0589 minus0087
Cumulativevariance 2687 5205 6528
SignificanceSpecies plt001 p = 001 p = 107
Significanceperchtype plt001 plt001 p = 002
Eigenvalue 2150 2015 1058
SignificanceforttestscomparingprincipalcomponentsbetweenA stratu-lusandA cristatellusaregivenintherowlabelledldquoSignificanceSpeciesrdquoandsignificanceforttestscomparingprincipalcomponentsbetweennatu-ralandmanmadeperchesaregivenintherowlabelledldquoSignificancePerchTyperdquoSignificantloadingsareboldedandshadedSignificancelevelsforspeciesandperchtypeANOVAsareplt001plt01
32emsp |emsp emspensp WINCHELL Et aL
dense or continuous canopy Moreover manmade substrates suchaswallsandfencesareclearlyvisibleall thewaytotherooflineAssuchvisibilityofthefewhighperchespresentwasverygoodacrossallurbansitesandwedonotexpectthatwefailedtoobserveasignif-icantnumberofindividualsathigherperches
42emsp|emspHabitat use
ThetwolizardspeciesofthisstudydifferedinthefrequencywhichtheyutilizedmanmadesubstratesasperchesAnolis cristatellususedman-madeperchesatahighfrequencybutusedbothmanmadestructuresandvegetationinproportiontotheirrelativeabundanceintheenviron-mentIncontrastA stratulusinfrequentlyoccupiedmanmadeperchesSimilarlyKolbeBattlesandAvileacutes-Rodriacuteguez(2015)foundthatA cris-tatellususedmanmadestructuresmorefrequentlythanA stratulus in human-modifiedhabitatsdespitefindingA stratulustobemoreadeptatsprintingonsmoothverticalsurfacesOurdatasuggestthatA stratu-luseitheractivelyseeksoutnaturalsubstratesoravoidstheuseofman-madesubstratesThispatternmaybeexplainedbysomecombinationofpredationcompetitionperformanceandhabitatrequirements
AtfirstglanceitappearsthatA cristatellusandA stratuluspartitionurbanniche space in similarwaysas innatural foresthabitatWhenfoundsyntopicallyinnaturalforesthabitatthesetwospeciesdividethehabitatsuchasmanyanolespeciesbasedprimarilyonstructuralandmicroclimatichabitatfeatures(Rand1964reviewedinLosos2009)InnaturalhabitatsA cristatellustypicallyusesbroaderandlowerpercheswhile A stratulususesthinnerandhigherperches(Cooper2005Rand
F IGURE 6emspPrincipalcomponents12and3plottedwith95confidenceintervalellipsesforutilizedhabitatbyeachspeciesPC1andPC2differedbetweenspeciesatsignificancelevelsplt001()andplt01()respectively
minus25
00
25
minus25 00 25 minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
A cristatellus
A stratulus
PC3
A cristatellus
A stratulus Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower perchesLess isolated perches
F IGURE 7emspPrincipalcomponents1and2plottedwith95confidenceintervalellipsesgroupedbyperchtypeforavailablehabitat(left)andutilizedhabitat(right)
Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower humidityHigher temperature (ambient amp perch)
A cristatellusManmade perches
A cristatellusNatural perches
A stratulusminus25
00
25
minus25 00 25
PC1
minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
Natural perches
Manmadeperches
TABLE 4emspResultsofANOVAandTukeyrsquosHSDcomparingprincipalcomponentsbetweenutilizedhabitatbyA stratulus(all)andA cristatellus(byperchtype)Degreesoffreedom(df)Fandp-value(p)aregivenforeachtest
ANOVA Tukeyrsquos HSD
df F p CNndashCM CNndashS CMndashS
PC1 286 24970 lt001 0313 001 lt001
PC2 286 28890 lt001 lt001 695 lt001
PC3 286 1323 272 1000 413 361
PairedcomparisonsfortheTukeyrsquosHSDtestsareA cristatellususingnatu-ralperchesversusA cristatellususingmanmadeperches(CNndashCM)A cris-tatellususingnaturalperchesversusA stratulusonallperches(CNndashS)andA cristatellus using manmade perches versus A stratulus on all perches(CMndashS)Significancelevelsplt001plt01plt05Significantre-sultsareboldedandshaded
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
emspensp emsp | emsp27WINCHELL Et aL
to be warmer and drier than nearby forests (reviewed in Forman2014)Wherethetwospeciesco-occurinnaturalforesthabitatstheypartitionthehabitatstructurallyandclimaticallySpecificallypriorre-search suggests thatA stratulus utilizeshigher and thinnerperchesandperchsitesthatarecoolerhigherinhumidityandhavemoreex-tensivecanopycovercomparedtohabitatusedbyA cristatellus(Rand1964Reagan1992)
Hereweaskhowthesetwospeciesutilizeandpartitionanovelhabitat urban areas Our null hypothesis is that theywill maintainniche partitioning and habitat choices in the samemanner as theydointhenaturalforesthabitatschoosingnaturalsubstratesthatfittheirpreferencesInotherwordsA stratuluswillseekouthigherthin-nercoolerpercheswiththickercanopycoverwhileA cristatellus will seekoutlowerbroaderwarmerpercheswiththinnercanopycoverAlternativelybothspeciesmayutilize thenovelnichespaceassoci-atedwithmanmadehabitat(ieonandaroundbuildings)Athirdpos-sibilityisthatonlyonespeciesexpandsintothenovelhabitatspaceassociated with anthropogenic resources while the other remainsstrictlyassociatedwithnaturalaspectsoftheurbanspace
WetestedthesehypothesesbymeasuringtherelativeabundancehabitatuseandnichespaceoccupiedbythesetwospeciesinurbanareasBecauseA cristatellus ismoreofageneralistwepredict thatitwilloccupyagreaterportionoftheurbanhabitatspaceandmoreextensively utilize habitat associatedwith anthropogenic structureswhile A stratuluswillremainassociatedwithnaturalhabitatelementsSimilartonaturalhabitatswealsopredictthateachspecieswillnon-randomlyutilizeperchesthatbestmeettheirstructuralandclimaticpreferencesasobserved innatural areasUnderstandingdifferentialhabitatuseinurbanpersistentspeciesshedslightonthefactorsinflu-encingurbantolerance(thegeneralcapacitytopersistinurbanareas)versusgenuineurbanophilyHereweprovideanempiricaltestofthisecological theoryMoreover this typeofnaturalhistory informationcanaidconservationinurbanareasbyidentifyingtheminimumhab-itat requirementsofnative species and thepotential forurbanper-sistenceandadaptation
2emsp |emspMATERIALS AND METHODS
From24April2015to6May2015wesampledsixurbansitesinfourmunicipalitiesinnorthernandwesternPuertoRicoSanJuanAreciboAguadilla and Mayaguumlez (Figure2a) In San Juan Aguadilla andMayaguumlez thesiteswereresidentialneighborhoods InArecibowesampledoneresidentialneighborhoodandtwouniversitycampuses(UniversityofPuertoRicoAreciboandUniversityInteramericana)ForlogisticalreasonswedidnotsamplenearbyforestedareasOurvisualsamplingmethodsusedintheurbanhabitatwouldlikelyhavebeenin-adequateinforesthabitatsduetothedifferencesinstructuralhabitatcomplexityandcanopyusebyA stratulus
Ateachlocalitywesampledabundancebyslowlywalkingthroughthehabitatforaminimumof3hrwithoutretracingourpathbetween8amand7pm(dusk)Becausethesespeciesvaryintheirhabitatusethroughoutthedayinnaturalforesthabitats(Hertz1992Nicholsonetal2005)andinurbanhabitats(Avileacutes-Rodriacuteguezunpublished data)surveyswereconductedatdifferenttimesofthedaywithatleastonesite surveyedduring each daylight hour (Figure2b) For every adultlizardobservedwerecordedspeciesandperchsubstrate
Wechosea subsetof theobserved lizardsas focalanimalsWeonlychosefocalanimalsoccupyinguniqueperchestoavoidaccidentalpseudoreplication(iewedidnotsamplemultiplelizardsofthesame
F IGURE 1emspAnolis cristatellus(topphotoEJC)andAnolis stratulus (bottomphotoKMW)occupydifferentportionsoftheurbanhabitat
(a)
(b)
28emsp |emsp emspensp WINCHELL Et aL
speciesutilizingthesametree)BecauseofdifferencesinabundancewesampledeveryA stratulusoccupyingauniqueperchandthenextobservedA cristatellus resulting inapproximatelyequalnumbersoffocalobservationsperspeciesForfocalanimalswenotedenviron-mentalconditionsandhabitatuseambienttemperature(digitalprobeOMEGAHH12B)perchtemperature(infraredprobeEXTECHIR201)relativehumidity(digitalmeterAMPROBETHWD-3)sunconditionsperchheightperchdiameterdistancetonearestpotentialperch(anystructureatleast05mhighandrobustenoughtosupporttheweightofanadultofeitherspecies)perchtypeandperchroughnessPerchroughnesswasratedonascaleof1ndash5withlowernumbersindicatingsmoothersubstratesRatingswereasfollows(basedonpreviousanal-ysesofsurfaceroughnessandsubstratetypeWinchelletal2016)(1)glass(2)metal(3)paintedconcrete(4)unpaintedprocessedwoodleaves and smooth bark trees such as bamboo and (5) thick barktreessuchasTababuya amarilloandCalophyllum antillanumaswellasunpainted andweathered concreteWe took photos of the canopyimmediatelyabovetheperchsite(OlympusEP5withOlympus9mm180fisheye)Weestimatedvegetativecanopycoverandmanmadecanopycover(iemanmadestructuresobscuringthesky)fromthesephotographsusingAdobePhotoshop(CS51)
Foreveryfocalanimalwealsosampledavailablehabitatbyran-domlyselectinganearbyperchWesamplednearbyavailableperchesbychoosingtheclosestpotentialperchinarandomdirectionfromthesampledperchWecollectedthesamehabitatmeasurementsasthosenotedaboveatthreeheights0515and2mabovethegroundre-sultinginasetofthreerandomperchesforeveryutilizedperchForpercheslt2minheightwesampledonlyat05and15mWallperches
greaterthan50cmindiameterwererecordedas100cmasdiametercannotbesensiblycalculatedforcompletely flatperches (egwalls)andperchesofthissizearelikelyfunctionallyequivalentforsmallliz-ards(egCartmill1985)Welog-transformedperchheightdiameteranddistancetonearestperchesbeforesubsequentstatisticalanalyses
Weanalyzeddifferences inhabitat choiceandniche spacewiththreemainanalysesWeperformedallstatisticalanalysesusingR322(RCoreTeam2015)Firstwetestedfordifferencesinhabitatutilizedbyeachspeciescomparedtotherandomlyavailablehabitat(iehab-itatchoice)byfittingatwo-wayMANOVAforeachspecieswithsiteandsamplenumber(toaccountforcorrelationbetweenavailablehab-itatsamples)ascovariates(residualsforthesemodelscanbefoundinthesupplementalmaterialsS1-S3)WeusedFisherrsquosExactandChi-square tests (as appropriate) to compare perch type used betweenspecies and between each species and randomly available perchesWedidnotincludeperchheightinthisanalysisaswedidnotrandomlysample available perches at the full range of potential heights (egaboveourreach)Secondwedeterminedkeyhabitatvariablesdistin-guishingperchoccupancybetweenthetwospeciesusingconditionalinferenceclassificationtreeanalysisThisanalysisdeterminespredic-tivevariableswiththegreatestexplanatorypowertoseparategroupsandprovidesthresholdestimatesforeachvariableWefitourclassifi-cationmodelusingtheRpackageldquopartyrdquo(HothornHornikampZeileis2006)Finallyweanalyzedhowthetwospeciespartitionthehabitatasawholewithavarimax-rotatedprincipalcomponentanalysisonthecorrelationmatrixforutilizedandavailablehabitatdatausingthevari-ables forwhichhabitatchoicewassuggestedbytheMANOVAsforat leastone speciesWe retainedcomponentswitheigenvaluesgt1
F IGURE 2emsp (a)LocationsofsitessampledInsetinArecibothreelocationsweresurveyed(indicatedbystars)(1)UniversityIneteramericanaArecibo(2)aresidentialneighborhoodand(3)UniversityofPuertoRicoAreciboDashedlinesindicatemajorhighways(thickdash)andmajorsurfaceroads(smalldash)(b)Distributionofhourssampledacrossallsites
Mayaguumlez
San Juan
AguadillaArecibo
0
1
2
3
4
5
8 9 10 11 12 13 14 15 16 17 18 19Time of day
Cou
nt
SiteAguadillaAreciboMayaguezSan JuanU InteramericanaUPR Arecibo
3
2
1
2 Kilometers
0 125 25 50 km
(a) (b)
emspensp emsp | emsp29WINCHELL Et aL
ForretainedcomponentswethencomparedmultidimensionalhabitatusebetweenspecieswithttestsandbetweenutilizedandavailablehabitatwithANOVAandTukeyrsquosHSDposthoctests
3emsp |emspRESULTS
Collectivelywespentatotalof64person-hoursat5urbansitesandrecorded487lizardsOfthese442wereA cristatellus(mean668liz-ards per person-hour per site) and45wereA stratulus (mean073lizardsperperson-hourpersite) Inadditionwesampled31 lizards(n = 20 A cristatellusandn = 11 A stratulus)fromasixthsite(AreciboUI)inwhichwedidnotrecordtotalsightingsOfthese518animalswe sampled a total of 47A stratulus and 52A cristatellus as focalanimalsforhabitatuseandtookatotalof274measuresofpotentialperchsites(ldquoavailablehabitatrdquo)
AssumingdetectionprobabilityissimilarforthetwospeciesA cri-statellusweresignificantlymoreabundantthanA stratulusacrosssites(FisherrsquosExactplt001Figure3a)ComparingallobservedanimalsfromthefivesitesinwhichwerecordedtotalsightingswefoundthatA cristatellus utilizedmanmade substrates such aswalls and fencesat a much higher rate (62) than A stratulus (4) (Fisherrsquos Exactplt001Figure3b)Howeverwhencomparingtheseobservationstoallrandomperchsites(n=96)wefoundthatA stratulususesnaturalsubstratesmorefrequentlythanencountered(FisherrsquosExactplt001)while A cristatellususesmanmadesubstratesatarelativefrequencysimilartotheiravailabilityintheenvironment(χ2p=535)
WefoundthatavailablehabitatdifferedsignificantlyfromutilizedhabitatforA cristatellusinfivevariablesambienttemperaturehumid-ityperchdiameterperchproximityandvegetativecanopycoverInA stratulusavailableandutilizedhabitatdifferedforsevenvariablesambienttemperatureperchtemperatureperchdiametervegetativecanopymanmadecanopyperchtypeandperchroughness(Tables1ndash2Figure4)
In terms of structural habitat (Table2 Figure4) A cristatellus perched lower than A stratulus (mean perch height A cristatellus 1080mmeanperchheightA stratulus1561mt=minus3293df=88p=001) Both species utilized thinner perches than are randomlyavailablewhich isunsurprisinggiventhe largenumberofextremelybroaddiameterperches inurbanareas (egwalls)Anolis cristatellus also chose perches that were less isolated (ie perches that werecloser toanalternateperchsite)whileA stratulusdidnotdiscrimi-nateonthisaxisInadditionA cristatellusdidnotdiscriminatelyusehabitatbasedonperchtype(manmadevsnatural)orsubstraterough-nesswhereasA stratulususednaturalperchesandperchesthathadroughersurfacesatahigherfrequencythanexpectedbasedontheiravailability
Intermsofmicroclimate(Table2Figure4)bothspeciesactivelyselectedmicrohabitatbasedonambienttemperaturethoughinoppo-sitedirectionsA cristatellusutilizedwarmerhabitatwhileA stratulus utilizedcoolerhabitatInadditionA cristatellususedperchesthathadlowerhumidityandA stratulususedperchesthathadlowersurfacetemperaturesAlthoughbothmanmade(shadecastbybuiltstructures)andvegetative(shadecastbytreesorothervegetation)canopycovers
F IGURE 3emsp (a)RelativeabundancesdiffereddramaticallyweencounteredmanymoreA cristatellusacrossallsites(b)AnoliscristatellususedartificialperchesatahigherfrequencythannaturalperchesandatasimilarratetowhatwasavailableAnolis stratulususednaturalperchesalmostexclusively(FisherrsquosExacttestplt001)
0
25
50
75
100
Aguadilla
Arecibo (res)
Arecibo (UPR)
Mayaguez
San Juan
Spe
cies
per
site
(
)
A cristatellusA stratulus
n = 85 n = 251 n = 18 n = 64 n = 54
0
25
50
75
100
A cristatellus
(use)
A stratulus(use)
Available
Per
ch u
se fr
eque
ncy
n = 442 n = 45 n = 96
Perch type
Manmade Natural
(a) (b)
30emsp |emsp emspensp WINCHELL Et aL
werelowacrossallsitesA stratulusdiscriminatelyutilizedperchsiteswithveryhighvegetativecanopycoverandverylowmanmadecovercompared to random perchesAnolis cristatellus also chose percheswithslightlyhighervegetativecanopythanexpectedbychancebutthiseffectwasrelativelyweakandA cristatellusdidnotappeartodis-criminatefororagainstmanmadecover
Wenextanalyzedspeciespresenceataperchsiteusingclassifi-cationtreeanalysistoidentifyhabitatfactorsthatdifferentiateperchappropriateness between the two species (Figure5) This analysis
revealed that habitat use inA stratulus andA cristatellus separatesbasedontwokeyvariablesThespeciesdifferedprimarily inhabitatusebasedonvegetativecanopycover(plt001)withthemajorityofA stratulususingperchescoveredbygreaterthan740treecoverand secondarily based on ambient temperature (p=009) with themajorityofA cristatellus usinghabitatwith lower canopycoverandambienttemperaturesgreaterthan293degC
Lastlyweanalyzedmulti-dimensionalnichespacewithavarimax-rotatedprincipal component analysis of thesehabitatvariablesWeincludedperchheightandsevenoftheeightsignificantvariablesfromtheMANOVAanalyses in thisanalysis todeterminedifferencesbe-tweenspecies inmultivariatenichespaceWe includedonlyoneofthecanopycovervariables(vegetativecanopy)becauseweareinter-estedindescribingnichespacewithoutanyexplicitlyurbanvariablesincluded (egmanmadecanopycover)Principalcomponents1and2were significantly different betweenA stratulus andA cristatellus (t test Table3 Figure6) and the first three principal componentscaptured653ofvarianceVarimax-rotatedcomponent1hadhighpositiveloadingsforambientandperch(surface)temperaturesandahighnegativeloadingforhumidityComponent2hadhighapositiveloadingforperchdiameterandhighnegativeloadingsforvegetativecanopy cover and perch roughness Finally component 3 had highnegativeloadingsforperchheightandproximitytonearestperch
Weanticipated thatmanyof the relevantenvironmental factorscould be associatedwith artificial substrates sowe also comparedmultidimensionalnichespaceofavailableandutilizedperchesassoci-atedwithnaturalandartificialsubstrates(Figure7)Availablehabitatdifferedbetweenartificialandnaturalperchtypesforallthreeprin-cipalcomponentssuggestingthathabitatassociatedwithmanmadeperchesdiffersfromthatassociatedwithnaturalperchesinmultipledimensions (Figure7Table3) Finallywe compared utilized habitatseparatedbyperchtypeforA cristatellustoutilizedhabitatforA strat-ulusWefoundthatmanmadeperchesusedbyA cristatellusdifferedfromnaturalperchesusedbyA cristatellusandfromallperchesusedbyA stratulusforPC1andPC2(Figure7Table4)suggestingthatdi-vergenceinhabitatusebetweenthespeciesisassociatedwiththeuseofmanmadeperches
4emsp |emspDISCUSSION
41emsp|emspAbundance
We found that A cristatellus was significantly more abundant thanA stratulusatsampledurbansitesInparticularweencounterednearly10timesasmanyA cristatellusasA stratulusacrossallsitesandtheformer specieswas encountered at amuch higher rate per person-hour This finding could simply be a consequence of differences inabundanceinnaturalhabitatsnearbyBothA cristatellusandA stratu-lusarelocallyabundantinnaturalhabitatsinPuertoRicowithsympat-ricdensitiesinmesichabitatsatgroundlevelestimatedat1000ndash1100and 600ndash900 per hectare respectively (Rodda Perry Rondeau ampLazell 2001) If fewerA stratulus are found innearbynatural areasthenwemightexpecturbanhabitatstoinheritthisnaturaldifference
TABLE 1emspResultsfromMANOVAsforhabitatuseversusavailabilityfortheninehabitatvariablescomparingthesixurbansitesandhabitatchoiceDegreesoffreedom(df)Fandp-value(p)aregivenforeach
Wilksrsquo lambda df F p
Anolis cristatellus
Habitatchoice 0569 1216 17459 lt001
Urbansite 0025 5216 26549 lt001
Anolis stratulus
Habitatchoice 0247 1212 68827 lt001
Urbansite 0010 5212 36574 lt001
Statistically significant values forhabitat choice areboldedand indicatedifferencesbetweenutilizedandrandomlyavailablehabitat
TABLE 2emspResultsfromANCOVAsforhabitatchoicesubsequenttotheMANOVAsinTable1Degreesoffreedom(df)Fandp-value(p)aregivenforeach
df F p
Anolis cristatellus
Ambienttemperature 1216 55822 lt001
Perchtemperature 1216 0331 566
Humidity 1216 99237 lt001
Perchheight 1216 5868 016
Perchdiameter 1216 9012 003
Perchproximity 1216 23067 lt001
Vegetativecanopy 1216 4028 046
Manmadecanopy 1216 1437 232
Perchroughness 1216 1589 209
Anolis stratulus
Ambienttemperature 1212 47060 lt001
Perchtemperature 1212 29113 lt001
Humidity 1212 2660 104
Perchheight 1212 0197 658
Perchdiameter 1212 40113 lt001
Perchproximity 1212 0187 666
Vegetativecanopy 1212 319157 lt001
Manmadecanopy 1212 104938 lt001
Perchroughness 1212 238820 lt001
Shadedcellsaresignificantfordifferencebetweenuseandavailabilityatthesignificancelevelindicatedbythelastcolumn
emspensp emsp | emsp31WINCHELL Et aL
inabundancebetweenspeciesHoweverthedifferenceinabundancesmeasured inthepresentstudyfarexceedsthatfoundpreviouslyforPuertoRicanmesicforest(egRoddaetal2001)ThissuggeststhaturbanhabitatsdonotsupportA stratulusandA cristatellusinrelativeabundances proportional to those reported for more natural sitesRelative abundances in urban areas instead appear to follow a pat-ternmorecloselyresemblingnaturallyxericforests(egGenetGenetBurtonampMurphy2001)despitebeinglocatedinmesicregions
ItispossiblethatoursamplingmethodmayhavefailedtodetectA stratulus perching higher in the urban canopy Indeed in naturalhabitatsA stratulus densityhasbeenunderestimatedat somesiteswhentheyutilizecanopyhabitatForexampleReagan(1992)found
thatA stratulusattainsextremelyhighdensities(24000ndash28000ha)inforestswhereindividualsoccupyhighcanopyhabitat(approximately10ndash20mheight)Webelievethisisnotamajorconcerninourstudyasurbantreesatoursitestendedtobeshorterandrarelyproduced
F IGURE 4emspMeanandSEforhabitatvariablessampledforhabitatavailability(ldquoArdquo)andeachspeciesuse(ldquoCrdquomdashA cristatellusldquoSrdquomdashA stratulus)Differencesbetweenutilizedandavailablehabitat(summarizedinTable2)representedbygraylinesandsignificancelevelplt001plt01plt05
Ambient temp (degC)
295
300
305
310
Manmade canopy ()
10
20
Perch height (cm)
44
46
48
50
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
Perch diameter (cm)
24
27
30
33
Nearest perch (cm)
46
48
50
52
Relative humidity ()
52
54
56
58
60
290
295
300
305
Veg canop y ()
40
50
60
70
80
(log
scal
e)
Surface roughness
35
40
45
Perch temp (degC)
F IGURE 5emspClassificationtreeforhabitatusedifferencesinA cristatellusandA stratulusSpeciespercentagesindicatethepercentageofallsampledindividualsofeachspeciesineachgroup(highcanopycoverlowcanopycoverandhightemperaturelowcanopycoverandlowtemperature)
Veg canopy p lt 0001
le7404 cover gt7404 cover
Ambient tempp = 0009
le293degC gt293degC
A cristatellus 58A stratulus 149
A cristatellus 712A stratulus 8 5
A cristatellus 231A stratulus 766
TABLE 3emspResultsfromvarimax-rotatedprinciplecomponentanalysisofurbanhabitat
PC1 PC2 PC3
Humidity minus0560 0118 minus0163
Ambienttemp 0616 minus0008 0010
Perchheight minus0112 minus0040 minus0571
Perchdiameter minus0188 0477 minus0048
Nearestperch 0136 0011 minus0786
Vegcanopy minus0125 minus0631 0014
Perchtemp 0473 0108 minus0136
Perchroughness minus0042 minus0589 minus0087
Cumulativevariance 2687 5205 6528
SignificanceSpecies plt001 p = 001 p = 107
Significanceperchtype plt001 plt001 p = 002
Eigenvalue 2150 2015 1058
SignificanceforttestscomparingprincipalcomponentsbetweenA stratu-lusandA cristatellusaregivenintherowlabelledldquoSignificanceSpeciesrdquoandsignificanceforttestscomparingprincipalcomponentsbetweennatu-ralandmanmadeperchesaregivenintherowlabelledldquoSignificancePerchTyperdquoSignificantloadingsareboldedandshadedSignificancelevelsforspeciesandperchtypeANOVAsareplt001plt01
32emsp |emsp emspensp WINCHELL Et aL
dense or continuous canopy Moreover manmade substrates suchaswallsandfencesareclearlyvisibleall thewaytotherooflineAssuchvisibilityofthefewhighperchespresentwasverygoodacrossallurbansitesandwedonotexpectthatwefailedtoobserveasignif-icantnumberofindividualsathigherperches
42emsp|emspHabitat use
ThetwolizardspeciesofthisstudydifferedinthefrequencywhichtheyutilizedmanmadesubstratesasperchesAnolis cristatellususedman-madeperchesatahighfrequencybutusedbothmanmadestructuresandvegetationinproportiontotheirrelativeabundanceintheenviron-mentIncontrastA stratulusinfrequentlyoccupiedmanmadeperchesSimilarlyKolbeBattlesandAvileacutes-Rodriacuteguez(2015)foundthatA cris-tatellususedmanmadestructuresmorefrequentlythanA stratulus in human-modifiedhabitatsdespitefindingA stratulustobemoreadeptatsprintingonsmoothverticalsurfacesOurdatasuggestthatA stratu-luseitheractivelyseeksoutnaturalsubstratesoravoidstheuseofman-madesubstratesThispatternmaybeexplainedbysomecombinationofpredationcompetitionperformanceandhabitatrequirements
AtfirstglanceitappearsthatA cristatellusandA stratuluspartitionurbanniche space in similarwaysas innatural foresthabitatWhenfoundsyntopicallyinnaturalforesthabitatthesetwospeciesdividethehabitatsuchasmanyanolespeciesbasedprimarilyonstructuralandmicroclimatichabitatfeatures(Rand1964reviewedinLosos2009)InnaturalhabitatsA cristatellustypicallyusesbroaderandlowerpercheswhile A stratulususesthinnerandhigherperches(Cooper2005Rand
F IGURE 6emspPrincipalcomponents12and3plottedwith95confidenceintervalellipsesforutilizedhabitatbyeachspeciesPC1andPC2differedbetweenspeciesatsignificancelevelsplt001()andplt01()respectively
minus25
00
25
minus25 00 25 minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
A cristatellus
A stratulus
PC3
A cristatellus
A stratulus Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower perchesLess isolated perches
F IGURE 7emspPrincipalcomponents1and2plottedwith95confidenceintervalellipsesgroupedbyperchtypeforavailablehabitat(left)andutilizedhabitat(right)
Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower humidityHigher temperature (ambient amp perch)
A cristatellusManmade perches
A cristatellusNatural perches
A stratulusminus25
00
25
minus25 00 25
PC1
minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
Natural perches
Manmadeperches
TABLE 4emspResultsofANOVAandTukeyrsquosHSDcomparingprincipalcomponentsbetweenutilizedhabitatbyA stratulus(all)andA cristatellus(byperchtype)Degreesoffreedom(df)Fandp-value(p)aregivenforeachtest
ANOVA Tukeyrsquos HSD
df F p CNndashCM CNndashS CMndashS
PC1 286 24970 lt001 0313 001 lt001
PC2 286 28890 lt001 lt001 695 lt001
PC3 286 1323 272 1000 413 361
PairedcomparisonsfortheTukeyrsquosHSDtestsareA cristatellususingnatu-ralperchesversusA cristatellususingmanmadeperches(CNndashCM)A cris-tatellususingnaturalperchesversusA stratulusonallperches(CNndashS)andA cristatellus using manmade perches versus A stratulus on all perches(CMndashS)Significancelevelsplt001plt01plt05Significantre-sultsareboldedandshaded
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
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AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
28emsp |emsp emspensp WINCHELL Et aL
speciesutilizingthesametree)BecauseofdifferencesinabundancewesampledeveryA stratulusoccupyingauniqueperchandthenextobservedA cristatellus resulting inapproximatelyequalnumbersoffocalobservationsperspeciesForfocalanimalswenotedenviron-mentalconditionsandhabitatuseambienttemperature(digitalprobeOMEGAHH12B)perchtemperature(infraredprobeEXTECHIR201)relativehumidity(digitalmeterAMPROBETHWD-3)sunconditionsperchheightperchdiameterdistancetonearestpotentialperch(anystructureatleast05mhighandrobustenoughtosupporttheweightofanadultofeitherspecies)perchtypeandperchroughnessPerchroughnesswasratedonascaleof1ndash5withlowernumbersindicatingsmoothersubstratesRatingswereasfollows(basedonpreviousanal-ysesofsurfaceroughnessandsubstratetypeWinchelletal2016)(1)glass(2)metal(3)paintedconcrete(4)unpaintedprocessedwoodleaves and smooth bark trees such as bamboo and (5) thick barktreessuchasTababuya amarilloandCalophyllum antillanumaswellasunpainted andweathered concreteWe took photos of the canopyimmediatelyabovetheperchsite(OlympusEP5withOlympus9mm180fisheye)Weestimatedvegetativecanopycoverandmanmadecanopycover(iemanmadestructuresobscuringthesky)fromthesephotographsusingAdobePhotoshop(CS51)
Foreveryfocalanimalwealsosampledavailablehabitatbyran-domlyselectinganearbyperchWesamplednearbyavailableperchesbychoosingtheclosestpotentialperchinarandomdirectionfromthesampledperchWecollectedthesamehabitatmeasurementsasthosenotedaboveatthreeheights0515and2mabovethegroundre-sultinginasetofthreerandomperchesforeveryutilizedperchForpercheslt2minheightwesampledonlyat05and15mWallperches
greaterthan50cmindiameterwererecordedas100cmasdiametercannotbesensiblycalculatedforcompletely flatperches (egwalls)andperchesofthissizearelikelyfunctionallyequivalentforsmallliz-ards(egCartmill1985)Welog-transformedperchheightdiameteranddistancetonearestperchesbeforesubsequentstatisticalanalyses
Weanalyzeddifferences inhabitat choiceandniche spacewiththreemainanalysesWeperformedallstatisticalanalysesusingR322(RCoreTeam2015)Firstwetestedfordifferencesinhabitatutilizedbyeachspeciescomparedtotherandomlyavailablehabitat(iehab-itatchoice)byfittingatwo-wayMANOVAforeachspecieswithsiteandsamplenumber(toaccountforcorrelationbetweenavailablehab-itatsamples)ascovariates(residualsforthesemodelscanbefoundinthesupplementalmaterialsS1-S3)WeusedFisherrsquosExactandChi-square tests (as appropriate) to compare perch type used betweenspecies and between each species and randomly available perchesWedidnotincludeperchheightinthisanalysisaswedidnotrandomlysample available perches at the full range of potential heights (egaboveourreach)Secondwedeterminedkeyhabitatvariablesdistin-guishingperchoccupancybetweenthetwospeciesusingconditionalinferenceclassificationtreeanalysisThisanalysisdeterminespredic-tivevariableswiththegreatestexplanatorypowertoseparategroupsandprovidesthresholdestimatesforeachvariableWefitourclassifi-cationmodelusingtheRpackageldquopartyrdquo(HothornHornikampZeileis2006)Finallyweanalyzedhowthetwospeciespartitionthehabitatasawholewithavarimax-rotatedprincipalcomponentanalysisonthecorrelationmatrixforutilizedandavailablehabitatdatausingthevari-ables forwhichhabitatchoicewassuggestedbytheMANOVAsforat leastone speciesWe retainedcomponentswitheigenvaluesgt1
F IGURE 2emsp (a)LocationsofsitessampledInsetinArecibothreelocationsweresurveyed(indicatedbystars)(1)UniversityIneteramericanaArecibo(2)aresidentialneighborhoodand(3)UniversityofPuertoRicoAreciboDashedlinesindicatemajorhighways(thickdash)andmajorsurfaceroads(smalldash)(b)Distributionofhourssampledacrossallsites
Mayaguumlez
San Juan
AguadillaArecibo
0
1
2
3
4
5
8 9 10 11 12 13 14 15 16 17 18 19Time of day
Cou
nt
SiteAguadillaAreciboMayaguezSan JuanU InteramericanaUPR Arecibo
3
2
1
2 Kilometers
0 125 25 50 km
(a) (b)
emspensp emsp | emsp29WINCHELL Et aL
ForretainedcomponentswethencomparedmultidimensionalhabitatusebetweenspecieswithttestsandbetweenutilizedandavailablehabitatwithANOVAandTukeyrsquosHSDposthoctests
3emsp |emspRESULTS
Collectivelywespentatotalof64person-hoursat5urbansitesandrecorded487lizardsOfthese442wereA cristatellus(mean668liz-ards per person-hour per site) and45wereA stratulus (mean073lizardsperperson-hourpersite) Inadditionwesampled31 lizards(n = 20 A cristatellusandn = 11 A stratulus)fromasixthsite(AreciboUI)inwhichwedidnotrecordtotalsightingsOfthese518animalswe sampled a total of 47A stratulus and 52A cristatellus as focalanimalsforhabitatuseandtookatotalof274measuresofpotentialperchsites(ldquoavailablehabitatrdquo)
AssumingdetectionprobabilityissimilarforthetwospeciesA cri-statellusweresignificantlymoreabundantthanA stratulusacrosssites(FisherrsquosExactplt001Figure3a)ComparingallobservedanimalsfromthefivesitesinwhichwerecordedtotalsightingswefoundthatA cristatellus utilizedmanmade substrates such aswalls and fencesat a much higher rate (62) than A stratulus (4) (Fisherrsquos Exactplt001Figure3b)Howeverwhencomparingtheseobservationstoallrandomperchsites(n=96)wefoundthatA stratulususesnaturalsubstratesmorefrequentlythanencountered(FisherrsquosExactplt001)while A cristatellususesmanmadesubstratesatarelativefrequencysimilartotheiravailabilityintheenvironment(χ2p=535)
WefoundthatavailablehabitatdifferedsignificantlyfromutilizedhabitatforA cristatellusinfivevariablesambienttemperaturehumid-ityperchdiameterperchproximityandvegetativecanopycoverInA stratulusavailableandutilizedhabitatdifferedforsevenvariablesambienttemperatureperchtemperatureperchdiametervegetativecanopymanmadecanopyperchtypeandperchroughness(Tables1ndash2Figure4)
In terms of structural habitat (Table2 Figure4) A cristatellus perched lower than A stratulus (mean perch height A cristatellus 1080mmeanperchheightA stratulus1561mt=minus3293df=88p=001) Both species utilized thinner perches than are randomlyavailablewhich isunsurprisinggiventhe largenumberofextremelybroaddiameterperches inurbanareas (egwalls)Anolis cristatellus also chose perches that were less isolated (ie perches that werecloser toanalternateperchsite)whileA stratulusdidnotdiscrimi-nateonthisaxisInadditionA cristatellusdidnotdiscriminatelyusehabitatbasedonperchtype(manmadevsnatural)orsubstraterough-nesswhereasA stratulususednaturalperchesandperchesthathadroughersurfacesatahigherfrequencythanexpectedbasedontheiravailability
Intermsofmicroclimate(Table2Figure4)bothspeciesactivelyselectedmicrohabitatbasedonambienttemperaturethoughinoppo-sitedirectionsA cristatellusutilizedwarmerhabitatwhileA stratulus utilizedcoolerhabitatInadditionA cristatellususedperchesthathadlowerhumidityandA stratulususedperchesthathadlowersurfacetemperaturesAlthoughbothmanmade(shadecastbybuiltstructures)andvegetative(shadecastbytreesorothervegetation)canopycovers
F IGURE 3emsp (a)RelativeabundancesdiffereddramaticallyweencounteredmanymoreA cristatellusacrossallsites(b)AnoliscristatellususedartificialperchesatahigherfrequencythannaturalperchesandatasimilarratetowhatwasavailableAnolis stratulususednaturalperchesalmostexclusively(FisherrsquosExacttestplt001)
0
25
50
75
100
Aguadilla
Arecibo (res)
Arecibo (UPR)
Mayaguez
San Juan
Spe
cies
per
site
(
)
A cristatellusA stratulus
n = 85 n = 251 n = 18 n = 64 n = 54
0
25
50
75
100
A cristatellus
(use)
A stratulus(use)
Available
Per
ch u
se fr
eque
ncy
n = 442 n = 45 n = 96
Perch type
Manmade Natural
(a) (b)
30emsp |emsp emspensp WINCHELL Et aL
werelowacrossallsitesA stratulusdiscriminatelyutilizedperchsiteswithveryhighvegetativecanopycoverandverylowmanmadecovercompared to random perchesAnolis cristatellus also chose percheswithslightlyhighervegetativecanopythanexpectedbychancebutthiseffectwasrelativelyweakandA cristatellusdidnotappeartodis-criminatefororagainstmanmadecover
Wenextanalyzedspeciespresenceataperchsiteusingclassifi-cationtreeanalysistoidentifyhabitatfactorsthatdifferentiateperchappropriateness between the two species (Figure5) This analysis
revealed that habitat use inA stratulus andA cristatellus separatesbasedontwokeyvariablesThespeciesdifferedprimarily inhabitatusebasedonvegetativecanopycover(plt001)withthemajorityofA stratulususingperchescoveredbygreaterthan740treecoverand secondarily based on ambient temperature (p=009) with themajorityofA cristatellus usinghabitatwith lower canopycoverandambienttemperaturesgreaterthan293degC
Lastlyweanalyzedmulti-dimensionalnichespacewithavarimax-rotatedprincipal component analysis of thesehabitatvariablesWeincludedperchheightandsevenoftheeightsignificantvariablesfromtheMANOVAanalyses in thisanalysis todeterminedifferencesbe-tweenspecies inmultivariatenichespaceWe includedonlyoneofthecanopycovervariables(vegetativecanopy)becauseweareinter-estedindescribingnichespacewithoutanyexplicitlyurbanvariablesincluded (egmanmadecanopycover)Principalcomponents1and2were significantly different betweenA stratulus andA cristatellus (t test Table3 Figure6) and the first three principal componentscaptured653ofvarianceVarimax-rotatedcomponent1hadhighpositiveloadingsforambientandperch(surface)temperaturesandahighnegativeloadingforhumidityComponent2hadhighapositiveloadingforperchdiameterandhighnegativeloadingsforvegetativecanopy cover and perch roughness Finally component 3 had highnegativeloadingsforperchheightandproximitytonearestperch
Weanticipated thatmanyof the relevantenvironmental factorscould be associatedwith artificial substrates sowe also comparedmultidimensionalnichespaceofavailableandutilizedperchesassoci-atedwithnaturalandartificialsubstrates(Figure7)Availablehabitatdifferedbetweenartificialandnaturalperchtypesforallthreeprin-cipalcomponentssuggestingthathabitatassociatedwithmanmadeperchesdiffersfromthatassociatedwithnaturalperchesinmultipledimensions (Figure7Table3) Finallywe compared utilized habitatseparatedbyperchtypeforA cristatellustoutilizedhabitatforA strat-ulusWefoundthatmanmadeperchesusedbyA cristatellusdifferedfromnaturalperchesusedbyA cristatellusandfromallperchesusedbyA stratulusforPC1andPC2(Figure7Table4)suggestingthatdi-vergenceinhabitatusebetweenthespeciesisassociatedwiththeuseofmanmadeperches
4emsp |emspDISCUSSION
41emsp|emspAbundance
We found that A cristatellus was significantly more abundant thanA stratulusatsampledurbansitesInparticularweencounterednearly10timesasmanyA cristatellusasA stratulusacrossallsitesandtheformer specieswas encountered at amuch higher rate per person-hour This finding could simply be a consequence of differences inabundanceinnaturalhabitatsnearbyBothA cristatellusandA stratu-lusarelocallyabundantinnaturalhabitatsinPuertoRicowithsympat-ricdensitiesinmesichabitatsatgroundlevelestimatedat1000ndash1100and 600ndash900 per hectare respectively (Rodda Perry Rondeau ampLazell 2001) If fewerA stratulus are found innearbynatural areasthenwemightexpecturbanhabitatstoinheritthisnaturaldifference
TABLE 1emspResultsfromMANOVAsforhabitatuseversusavailabilityfortheninehabitatvariablescomparingthesixurbansitesandhabitatchoiceDegreesoffreedom(df)Fandp-value(p)aregivenforeach
Wilksrsquo lambda df F p
Anolis cristatellus
Habitatchoice 0569 1216 17459 lt001
Urbansite 0025 5216 26549 lt001
Anolis stratulus
Habitatchoice 0247 1212 68827 lt001
Urbansite 0010 5212 36574 lt001
Statistically significant values forhabitat choice areboldedand indicatedifferencesbetweenutilizedandrandomlyavailablehabitat
TABLE 2emspResultsfromANCOVAsforhabitatchoicesubsequenttotheMANOVAsinTable1Degreesoffreedom(df)Fandp-value(p)aregivenforeach
df F p
Anolis cristatellus
Ambienttemperature 1216 55822 lt001
Perchtemperature 1216 0331 566
Humidity 1216 99237 lt001
Perchheight 1216 5868 016
Perchdiameter 1216 9012 003
Perchproximity 1216 23067 lt001
Vegetativecanopy 1216 4028 046
Manmadecanopy 1216 1437 232
Perchroughness 1216 1589 209
Anolis stratulus
Ambienttemperature 1212 47060 lt001
Perchtemperature 1212 29113 lt001
Humidity 1212 2660 104
Perchheight 1212 0197 658
Perchdiameter 1212 40113 lt001
Perchproximity 1212 0187 666
Vegetativecanopy 1212 319157 lt001
Manmadecanopy 1212 104938 lt001
Perchroughness 1212 238820 lt001
Shadedcellsaresignificantfordifferencebetweenuseandavailabilityatthesignificancelevelindicatedbythelastcolumn
emspensp emsp | emsp31WINCHELL Et aL
inabundancebetweenspeciesHoweverthedifferenceinabundancesmeasured inthepresentstudyfarexceedsthatfoundpreviouslyforPuertoRicanmesicforest(egRoddaetal2001)ThissuggeststhaturbanhabitatsdonotsupportA stratulusandA cristatellusinrelativeabundances proportional to those reported for more natural sitesRelative abundances in urban areas instead appear to follow a pat-ternmorecloselyresemblingnaturallyxericforests(egGenetGenetBurtonampMurphy2001)despitebeinglocatedinmesicregions
ItispossiblethatoursamplingmethodmayhavefailedtodetectA stratulus perching higher in the urban canopy Indeed in naturalhabitatsA stratulus densityhasbeenunderestimatedat somesiteswhentheyutilizecanopyhabitatForexampleReagan(1992)found
thatA stratulusattainsextremelyhighdensities(24000ndash28000ha)inforestswhereindividualsoccupyhighcanopyhabitat(approximately10ndash20mheight)Webelievethisisnotamajorconcerninourstudyasurbantreesatoursitestendedtobeshorterandrarelyproduced
F IGURE 4emspMeanandSEforhabitatvariablessampledforhabitatavailability(ldquoArdquo)andeachspeciesuse(ldquoCrdquomdashA cristatellusldquoSrdquomdashA stratulus)Differencesbetweenutilizedandavailablehabitat(summarizedinTable2)representedbygraylinesandsignificancelevelplt001plt01plt05
Ambient temp (degC)
295
300
305
310
Manmade canopy ()
10
20
Perch height (cm)
44
46
48
50
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
Perch diameter (cm)
24
27
30
33
Nearest perch (cm)
46
48
50
52
Relative humidity ()
52
54
56
58
60
290
295
300
305
Veg canop y ()
40
50
60
70
80
(log
scal
e)
Surface roughness
35
40
45
Perch temp (degC)
F IGURE 5emspClassificationtreeforhabitatusedifferencesinA cristatellusandA stratulusSpeciespercentagesindicatethepercentageofallsampledindividualsofeachspeciesineachgroup(highcanopycoverlowcanopycoverandhightemperaturelowcanopycoverandlowtemperature)
Veg canopy p lt 0001
le7404 cover gt7404 cover
Ambient tempp = 0009
le293degC gt293degC
A cristatellus 58A stratulus 149
A cristatellus 712A stratulus 8 5
A cristatellus 231A stratulus 766
TABLE 3emspResultsfromvarimax-rotatedprinciplecomponentanalysisofurbanhabitat
PC1 PC2 PC3
Humidity minus0560 0118 minus0163
Ambienttemp 0616 minus0008 0010
Perchheight minus0112 minus0040 minus0571
Perchdiameter minus0188 0477 minus0048
Nearestperch 0136 0011 minus0786
Vegcanopy minus0125 minus0631 0014
Perchtemp 0473 0108 minus0136
Perchroughness minus0042 minus0589 minus0087
Cumulativevariance 2687 5205 6528
SignificanceSpecies plt001 p = 001 p = 107
Significanceperchtype plt001 plt001 p = 002
Eigenvalue 2150 2015 1058
SignificanceforttestscomparingprincipalcomponentsbetweenA stratu-lusandA cristatellusaregivenintherowlabelledldquoSignificanceSpeciesrdquoandsignificanceforttestscomparingprincipalcomponentsbetweennatu-ralandmanmadeperchesaregivenintherowlabelledldquoSignificancePerchTyperdquoSignificantloadingsareboldedandshadedSignificancelevelsforspeciesandperchtypeANOVAsareplt001plt01
32emsp |emsp emspensp WINCHELL Et aL
dense or continuous canopy Moreover manmade substrates suchaswallsandfencesareclearlyvisibleall thewaytotherooflineAssuchvisibilityofthefewhighperchespresentwasverygoodacrossallurbansitesandwedonotexpectthatwefailedtoobserveasignif-icantnumberofindividualsathigherperches
42emsp|emspHabitat use
ThetwolizardspeciesofthisstudydifferedinthefrequencywhichtheyutilizedmanmadesubstratesasperchesAnolis cristatellususedman-madeperchesatahighfrequencybutusedbothmanmadestructuresandvegetationinproportiontotheirrelativeabundanceintheenviron-mentIncontrastA stratulusinfrequentlyoccupiedmanmadeperchesSimilarlyKolbeBattlesandAvileacutes-Rodriacuteguez(2015)foundthatA cris-tatellususedmanmadestructuresmorefrequentlythanA stratulus in human-modifiedhabitatsdespitefindingA stratulustobemoreadeptatsprintingonsmoothverticalsurfacesOurdatasuggestthatA stratu-luseitheractivelyseeksoutnaturalsubstratesoravoidstheuseofman-madesubstratesThispatternmaybeexplainedbysomecombinationofpredationcompetitionperformanceandhabitatrequirements
AtfirstglanceitappearsthatA cristatellusandA stratuluspartitionurbanniche space in similarwaysas innatural foresthabitatWhenfoundsyntopicallyinnaturalforesthabitatthesetwospeciesdividethehabitatsuchasmanyanolespeciesbasedprimarilyonstructuralandmicroclimatichabitatfeatures(Rand1964reviewedinLosos2009)InnaturalhabitatsA cristatellustypicallyusesbroaderandlowerpercheswhile A stratulususesthinnerandhigherperches(Cooper2005Rand
F IGURE 6emspPrincipalcomponents12and3plottedwith95confidenceintervalellipsesforutilizedhabitatbyeachspeciesPC1andPC2differedbetweenspeciesatsignificancelevelsplt001()andplt01()respectively
minus25
00
25
minus25 00 25 minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
A cristatellus
A stratulus
PC3
A cristatellus
A stratulus Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower perchesLess isolated perches
F IGURE 7emspPrincipalcomponents1and2plottedwith95confidenceintervalellipsesgroupedbyperchtypeforavailablehabitat(left)andutilizedhabitat(right)
Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower humidityHigher temperature (ambient amp perch)
A cristatellusManmade perches
A cristatellusNatural perches
A stratulusminus25
00
25
minus25 00 25
PC1
minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
Natural perches
Manmadeperches
TABLE 4emspResultsofANOVAandTukeyrsquosHSDcomparingprincipalcomponentsbetweenutilizedhabitatbyA stratulus(all)andA cristatellus(byperchtype)Degreesoffreedom(df)Fandp-value(p)aregivenforeachtest
ANOVA Tukeyrsquos HSD
df F p CNndashCM CNndashS CMndashS
PC1 286 24970 lt001 0313 001 lt001
PC2 286 28890 lt001 lt001 695 lt001
PC3 286 1323 272 1000 413 361
PairedcomparisonsfortheTukeyrsquosHSDtestsareA cristatellususingnatu-ralperchesversusA cristatellususingmanmadeperches(CNndashCM)A cris-tatellususingnaturalperchesversusA stratulusonallperches(CNndashS)andA cristatellus using manmade perches versus A stratulus on all perches(CMndashS)Significancelevelsplt001plt01plt05Significantre-sultsareboldedandshaded
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
emspensp emsp | emsp29WINCHELL Et aL
ForretainedcomponentswethencomparedmultidimensionalhabitatusebetweenspecieswithttestsandbetweenutilizedandavailablehabitatwithANOVAandTukeyrsquosHSDposthoctests
3emsp |emspRESULTS
Collectivelywespentatotalof64person-hoursat5urbansitesandrecorded487lizardsOfthese442wereA cristatellus(mean668liz-ards per person-hour per site) and45wereA stratulus (mean073lizardsperperson-hourpersite) Inadditionwesampled31 lizards(n = 20 A cristatellusandn = 11 A stratulus)fromasixthsite(AreciboUI)inwhichwedidnotrecordtotalsightingsOfthese518animalswe sampled a total of 47A stratulus and 52A cristatellus as focalanimalsforhabitatuseandtookatotalof274measuresofpotentialperchsites(ldquoavailablehabitatrdquo)
AssumingdetectionprobabilityissimilarforthetwospeciesA cri-statellusweresignificantlymoreabundantthanA stratulusacrosssites(FisherrsquosExactplt001Figure3a)ComparingallobservedanimalsfromthefivesitesinwhichwerecordedtotalsightingswefoundthatA cristatellus utilizedmanmade substrates such aswalls and fencesat a much higher rate (62) than A stratulus (4) (Fisherrsquos Exactplt001Figure3b)Howeverwhencomparingtheseobservationstoallrandomperchsites(n=96)wefoundthatA stratulususesnaturalsubstratesmorefrequentlythanencountered(FisherrsquosExactplt001)while A cristatellususesmanmadesubstratesatarelativefrequencysimilartotheiravailabilityintheenvironment(χ2p=535)
WefoundthatavailablehabitatdifferedsignificantlyfromutilizedhabitatforA cristatellusinfivevariablesambienttemperaturehumid-ityperchdiameterperchproximityandvegetativecanopycoverInA stratulusavailableandutilizedhabitatdifferedforsevenvariablesambienttemperatureperchtemperatureperchdiametervegetativecanopymanmadecanopyperchtypeandperchroughness(Tables1ndash2Figure4)
In terms of structural habitat (Table2 Figure4) A cristatellus perched lower than A stratulus (mean perch height A cristatellus 1080mmeanperchheightA stratulus1561mt=minus3293df=88p=001) Both species utilized thinner perches than are randomlyavailablewhich isunsurprisinggiventhe largenumberofextremelybroaddiameterperches inurbanareas (egwalls)Anolis cristatellus also chose perches that were less isolated (ie perches that werecloser toanalternateperchsite)whileA stratulusdidnotdiscrimi-nateonthisaxisInadditionA cristatellusdidnotdiscriminatelyusehabitatbasedonperchtype(manmadevsnatural)orsubstraterough-nesswhereasA stratulususednaturalperchesandperchesthathadroughersurfacesatahigherfrequencythanexpectedbasedontheiravailability
Intermsofmicroclimate(Table2Figure4)bothspeciesactivelyselectedmicrohabitatbasedonambienttemperaturethoughinoppo-sitedirectionsA cristatellusutilizedwarmerhabitatwhileA stratulus utilizedcoolerhabitatInadditionA cristatellususedperchesthathadlowerhumidityandA stratulususedperchesthathadlowersurfacetemperaturesAlthoughbothmanmade(shadecastbybuiltstructures)andvegetative(shadecastbytreesorothervegetation)canopycovers
F IGURE 3emsp (a)RelativeabundancesdiffereddramaticallyweencounteredmanymoreA cristatellusacrossallsites(b)AnoliscristatellususedartificialperchesatahigherfrequencythannaturalperchesandatasimilarratetowhatwasavailableAnolis stratulususednaturalperchesalmostexclusively(FisherrsquosExacttestplt001)
0
25
50
75
100
Aguadilla
Arecibo (res)
Arecibo (UPR)
Mayaguez
San Juan
Spe
cies
per
site
(
)
A cristatellusA stratulus
n = 85 n = 251 n = 18 n = 64 n = 54
0
25
50
75
100
A cristatellus
(use)
A stratulus(use)
Available
Per
ch u
se fr
eque
ncy
n = 442 n = 45 n = 96
Perch type
Manmade Natural
(a) (b)
30emsp |emsp emspensp WINCHELL Et aL
werelowacrossallsitesA stratulusdiscriminatelyutilizedperchsiteswithveryhighvegetativecanopycoverandverylowmanmadecovercompared to random perchesAnolis cristatellus also chose percheswithslightlyhighervegetativecanopythanexpectedbychancebutthiseffectwasrelativelyweakandA cristatellusdidnotappeartodis-criminatefororagainstmanmadecover
Wenextanalyzedspeciespresenceataperchsiteusingclassifi-cationtreeanalysistoidentifyhabitatfactorsthatdifferentiateperchappropriateness between the two species (Figure5) This analysis
revealed that habitat use inA stratulus andA cristatellus separatesbasedontwokeyvariablesThespeciesdifferedprimarily inhabitatusebasedonvegetativecanopycover(plt001)withthemajorityofA stratulususingperchescoveredbygreaterthan740treecoverand secondarily based on ambient temperature (p=009) with themajorityofA cristatellus usinghabitatwith lower canopycoverandambienttemperaturesgreaterthan293degC
Lastlyweanalyzedmulti-dimensionalnichespacewithavarimax-rotatedprincipal component analysis of thesehabitatvariablesWeincludedperchheightandsevenoftheeightsignificantvariablesfromtheMANOVAanalyses in thisanalysis todeterminedifferencesbe-tweenspecies inmultivariatenichespaceWe includedonlyoneofthecanopycovervariables(vegetativecanopy)becauseweareinter-estedindescribingnichespacewithoutanyexplicitlyurbanvariablesincluded (egmanmadecanopycover)Principalcomponents1and2were significantly different betweenA stratulus andA cristatellus (t test Table3 Figure6) and the first three principal componentscaptured653ofvarianceVarimax-rotatedcomponent1hadhighpositiveloadingsforambientandperch(surface)temperaturesandahighnegativeloadingforhumidityComponent2hadhighapositiveloadingforperchdiameterandhighnegativeloadingsforvegetativecanopy cover and perch roughness Finally component 3 had highnegativeloadingsforperchheightandproximitytonearestperch
Weanticipated thatmanyof the relevantenvironmental factorscould be associatedwith artificial substrates sowe also comparedmultidimensionalnichespaceofavailableandutilizedperchesassoci-atedwithnaturalandartificialsubstrates(Figure7)Availablehabitatdifferedbetweenartificialandnaturalperchtypesforallthreeprin-cipalcomponentssuggestingthathabitatassociatedwithmanmadeperchesdiffersfromthatassociatedwithnaturalperchesinmultipledimensions (Figure7Table3) Finallywe compared utilized habitatseparatedbyperchtypeforA cristatellustoutilizedhabitatforA strat-ulusWefoundthatmanmadeperchesusedbyA cristatellusdifferedfromnaturalperchesusedbyA cristatellusandfromallperchesusedbyA stratulusforPC1andPC2(Figure7Table4)suggestingthatdi-vergenceinhabitatusebetweenthespeciesisassociatedwiththeuseofmanmadeperches
4emsp |emspDISCUSSION
41emsp|emspAbundance
We found that A cristatellus was significantly more abundant thanA stratulusatsampledurbansitesInparticularweencounterednearly10timesasmanyA cristatellusasA stratulusacrossallsitesandtheformer specieswas encountered at amuch higher rate per person-hour This finding could simply be a consequence of differences inabundanceinnaturalhabitatsnearbyBothA cristatellusandA stratu-lusarelocallyabundantinnaturalhabitatsinPuertoRicowithsympat-ricdensitiesinmesichabitatsatgroundlevelestimatedat1000ndash1100and 600ndash900 per hectare respectively (Rodda Perry Rondeau ampLazell 2001) If fewerA stratulus are found innearbynatural areasthenwemightexpecturbanhabitatstoinheritthisnaturaldifference
TABLE 1emspResultsfromMANOVAsforhabitatuseversusavailabilityfortheninehabitatvariablescomparingthesixurbansitesandhabitatchoiceDegreesoffreedom(df)Fandp-value(p)aregivenforeach
Wilksrsquo lambda df F p
Anolis cristatellus
Habitatchoice 0569 1216 17459 lt001
Urbansite 0025 5216 26549 lt001
Anolis stratulus
Habitatchoice 0247 1212 68827 lt001
Urbansite 0010 5212 36574 lt001
Statistically significant values forhabitat choice areboldedand indicatedifferencesbetweenutilizedandrandomlyavailablehabitat
TABLE 2emspResultsfromANCOVAsforhabitatchoicesubsequenttotheMANOVAsinTable1Degreesoffreedom(df)Fandp-value(p)aregivenforeach
df F p
Anolis cristatellus
Ambienttemperature 1216 55822 lt001
Perchtemperature 1216 0331 566
Humidity 1216 99237 lt001
Perchheight 1216 5868 016
Perchdiameter 1216 9012 003
Perchproximity 1216 23067 lt001
Vegetativecanopy 1216 4028 046
Manmadecanopy 1216 1437 232
Perchroughness 1216 1589 209
Anolis stratulus
Ambienttemperature 1212 47060 lt001
Perchtemperature 1212 29113 lt001
Humidity 1212 2660 104
Perchheight 1212 0197 658
Perchdiameter 1212 40113 lt001
Perchproximity 1212 0187 666
Vegetativecanopy 1212 319157 lt001
Manmadecanopy 1212 104938 lt001
Perchroughness 1212 238820 lt001
Shadedcellsaresignificantfordifferencebetweenuseandavailabilityatthesignificancelevelindicatedbythelastcolumn
emspensp emsp | emsp31WINCHELL Et aL
inabundancebetweenspeciesHoweverthedifferenceinabundancesmeasured inthepresentstudyfarexceedsthatfoundpreviouslyforPuertoRicanmesicforest(egRoddaetal2001)ThissuggeststhaturbanhabitatsdonotsupportA stratulusandA cristatellusinrelativeabundances proportional to those reported for more natural sitesRelative abundances in urban areas instead appear to follow a pat-ternmorecloselyresemblingnaturallyxericforests(egGenetGenetBurtonampMurphy2001)despitebeinglocatedinmesicregions
ItispossiblethatoursamplingmethodmayhavefailedtodetectA stratulus perching higher in the urban canopy Indeed in naturalhabitatsA stratulus densityhasbeenunderestimatedat somesiteswhentheyutilizecanopyhabitatForexampleReagan(1992)found
thatA stratulusattainsextremelyhighdensities(24000ndash28000ha)inforestswhereindividualsoccupyhighcanopyhabitat(approximately10ndash20mheight)Webelievethisisnotamajorconcerninourstudyasurbantreesatoursitestendedtobeshorterandrarelyproduced
F IGURE 4emspMeanandSEforhabitatvariablessampledforhabitatavailability(ldquoArdquo)andeachspeciesuse(ldquoCrdquomdashA cristatellusldquoSrdquomdashA stratulus)Differencesbetweenutilizedandavailablehabitat(summarizedinTable2)representedbygraylinesandsignificancelevelplt001plt01plt05
Ambient temp (degC)
295
300
305
310
Manmade canopy ()
10
20
Perch height (cm)
44
46
48
50
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
Perch diameter (cm)
24
27
30
33
Nearest perch (cm)
46
48
50
52
Relative humidity ()
52
54
56
58
60
290
295
300
305
Veg canop y ()
40
50
60
70
80
(log
scal
e)
Surface roughness
35
40
45
Perch temp (degC)
F IGURE 5emspClassificationtreeforhabitatusedifferencesinA cristatellusandA stratulusSpeciespercentagesindicatethepercentageofallsampledindividualsofeachspeciesineachgroup(highcanopycoverlowcanopycoverandhightemperaturelowcanopycoverandlowtemperature)
Veg canopy p lt 0001
le7404 cover gt7404 cover
Ambient tempp = 0009
le293degC gt293degC
A cristatellus 58A stratulus 149
A cristatellus 712A stratulus 8 5
A cristatellus 231A stratulus 766
TABLE 3emspResultsfromvarimax-rotatedprinciplecomponentanalysisofurbanhabitat
PC1 PC2 PC3
Humidity minus0560 0118 minus0163
Ambienttemp 0616 minus0008 0010
Perchheight minus0112 minus0040 minus0571
Perchdiameter minus0188 0477 minus0048
Nearestperch 0136 0011 minus0786
Vegcanopy minus0125 minus0631 0014
Perchtemp 0473 0108 minus0136
Perchroughness minus0042 minus0589 minus0087
Cumulativevariance 2687 5205 6528
SignificanceSpecies plt001 p = 001 p = 107
Significanceperchtype plt001 plt001 p = 002
Eigenvalue 2150 2015 1058
SignificanceforttestscomparingprincipalcomponentsbetweenA stratu-lusandA cristatellusaregivenintherowlabelledldquoSignificanceSpeciesrdquoandsignificanceforttestscomparingprincipalcomponentsbetweennatu-ralandmanmadeperchesaregivenintherowlabelledldquoSignificancePerchTyperdquoSignificantloadingsareboldedandshadedSignificancelevelsforspeciesandperchtypeANOVAsareplt001plt01
32emsp |emsp emspensp WINCHELL Et aL
dense or continuous canopy Moreover manmade substrates suchaswallsandfencesareclearlyvisibleall thewaytotherooflineAssuchvisibilityofthefewhighperchespresentwasverygoodacrossallurbansitesandwedonotexpectthatwefailedtoobserveasignif-icantnumberofindividualsathigherperches
42emsp|emspHabitat use
ThetwolizardspeciesofthisstudydifferedinthefrequencywhichtheyutilizedmanmadesubstratesasperchesAnolis cristatellususedman-madeperchesatahighfrequencybutusedbothmanmadestructuresandvegetationinproportiontotheirrelativeabundanceintheenviron-mentIncontrastA stratulusinfrequentlyoccupiedmanmadeperchesSimilarlyKolbeBattlesandAvileacutes-Rodriacuteguez(2015)foundthatA cris-tatellususedmanmadestructuresmorefrequentlythanA stratulus in human-modifiedhabitatsdespitefindingA stratulustobemoreadeptatsprintingonsmoothverticalsurfacesOurdatasuggestthatA stratu-luseitheractivelyseeksoutnaturalsubstratesoravoidstheuseofman-madesubstratesThispatternmaybeexplainedbysomecombinationofpredationcompetitionperformanceandhabitatrequirements
AtfirstglanceitappearsthatA cristatellusandA stratuluspartitionurbanniche space in similarwaysas innatural foresthabitatWhenfoundsyntopicallyinnaturalforesthabitatthesetwospeciesdividethehabitatsuchasmanyanolespeciesbasedprimarilyonstructuralandmicroclimatichabitatfeatures(Rand1964reviewedinLosos2009)InnaturalhabitatsA cristatellustypicallyusesbroaderandlowerpercheswhile A stratulususesthinnerandhigherperches(Cooper2005Rand
F IGURE 6emspPrincipalcomponents12and3plottedwith95confidenceintervalellipsesforutilizedhabitatbyeachspeciesPC1andPC2differedbetweenspeciesatsignificancelevelsplt001()andplt01()respectively
minus25
00
25
minus25 00 25 minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
A cristatellus
A stratulus
PC3
A cristatellus
A stratulus Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower perchesLess isolated perches
F IGURE 7emspPrincipalcomponents1and2plottedwith95confidenceintervalellipsesgroupedbyperchtypeforavailablehabitat(left)andutilizedhabitat(right)
Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower humidityHigher temperature (ambient amp perch)
A cristatellusManmade perches
A cristatellusNatural perches
A stratulusminus25
00
25
minus25 00 25
PC1
minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
Natural perches
Manmadeperches
TABLE 4emspResultsofANOVAandTukeyrsquosHSDcomparingprincipalcomponentsbetweenutilizedhabitatbyA stratulus(all)andA cristatellus(byperchtype)Degreesoffreedom(df)Fandp-value(p)aregivenforeachtest
ANOVA Tukeyrsquos HSD
df F p CNndashCM CNndashS CMndashS
PC1 286 24970 lt001 0313 001 lt001
PC2 286 28890 lt001 lt001 695 lt001
PC3 286 1323 272 1000 413 361
PairedcomparisonsfortheTukeyrsquosHSDtestsareA cristatellususingnatu-ralperchesversusA cristatellususingmanmadeperches(CNndashCM)A cris-tatellususingnaturalperchesversusA stratulusonallperches(CNndashS)andA cristatellus using manmade perches versus A stratulus on all perches(CMndashS)Significancelevelsplt001plt01plt05Significantre-sultsareboldedandshaded
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
30emsp |emsp emspensp WINCHELL Et aL
werelowacrossallsitesA stratulusdiscriminatelyutilizedperchsiteswithveryhighvegetativecanopycoverandverylowmanmadecovercompared to random perchesAnolis cristatellus also chose percheswithslightlyhighervegetativecanopythanexpectedbychancebutthiseffectwasrelativelyweakandA cristatellusdidnotappeartodis-criminatefororagainstmanmadecover
Wenextanalyzedspeciespresenceataperchsiteusingclassifi-cationtreeanalysistoidentifyhabitatfactorsthatdifferentiateperchappropriateness between the two species (Figure5) This analysis
revealed that habitat use inA stratulus andA cristatellus separatesbasedontwokeyvariablesThespeciesdifferedprimarily inhabitatusebasedonvegetativecanopycover(plt001)withthemajorityofA stratulususingperchescoveredbygreaterthan740treecoverand secondarily based on ambient temperature (p=009) with themajorityofA cristatellus usinghabitatwith lower canopycoverandambienttemperaturesgreaterthan293degC
Lastlyweanalyzedmulti-dimensionalnichespacewithavarimax-rotatedprincipal component analysis of thesehabitatvariablesWeincludedperchheightandsevenoftheeightsignificantvariablesfromtheMANOVAanalyses in thisanalysis todeterminedifferencesbe-tweenspecies inmultivariatenichespaceWe includedonlyoneofthecanopycovervariables(vegetativecanopy)becauseweareinter-estedindescribingnichespacewithoutanyexplicitlyurbanvariablesincluded (egmanmadecanopycover)Principalcomponents1and2were significantly different betweenA stratulus andA cristatellus (t test Table3 Figure6) and the first three principal componentscaptured653ofvarianceVarimax-rotatedcomponent1hadhighpositiveloadingsforambientandperch(surface)temperaturesandahighnegativeloadingforhumidityComponent2hadhighapositiveloadingforperchdiameterandhighnegativeloadingsforvegetativecanopy cover and perch roughness Finally component 3 had highnegativeloadingsforperchheightandproximitytonearestperch
Weanticipated thatmanyof the relevantenvironmental factorscould be associatedwith artificial substrates sowe also comparedmultidimensionalnichespaceofavailableandutilizedperchesassoci-atedwithnaturalandartificialsubstrates(Figure7)Availablehabitatdifferedbetweenartificialandnaturalperchtypesforallthreeprin-cipalcomponentssuggestingthathabitatassociatedwithmanmadeperchesdiffersfromthatassociatedwithnaturalperchesinmultipledimensions (Figure7Table3) Finallywe compared utilized habitatseparatedbyperchtypeforA cristatellustoutilizedhabitatforA strat-ulusWefoundthatmanmadeperchesusedbyA cristatellusdifferedfromnaturalperchesusedbyA cristatellusandfromallperchesusedbyA stratulusforPC1andPC2(Figure7Table4)suggestingthatdi-vergenceinhabitatusebetweenthespeciesisassociatedwiththeuseofmanmadeperches
4emsp |emspDISCUSSION
41emsp|emspAbundance
We found that A cristatellus was significantly more abundant thanA stratulusatsampledurbansitesInparticularweencounterednearly10timesasmanyA cristatellusasA stratulusacrossallsitesandtheformer specieswas encountered at amuch higher rate per person-hour This finding could simply be a consequence of differences inabundanceinnaturalhabitatsnearbyBothA cristatellusandA stratu-lusarelocallyabundantinnaturalhabitatsinPuertoRicowithsympat-ricdensitiesinmesichabitatsatgroundlevelestimatedat1000ndash1100and 600ndash900 per hectare respectively (Rodda Perry Rondeau ampLazell 2001) If fewerA stratulus are found innearbynatural areasthenwemightexpecturbanhabitatstoinheritthisnaturaldifference
TABLE 1emspResultsfromMANOVAsforhabitatuseversusavailabilityfortheninehabitatvariablescomparingthesixurbansitesandhabitatchoiceDegreesoffreedom(df)Fandp-value(p)aregivenforeach
Wilksrsquo lambda df F p
Anolis cristatellus
Habitatchoice 0569 1216 17459 lt001
Urbansite 0025 5216 26549 lt001
Anolis stratulus
Habitatchoice 0247 1212 68827 lt001
Urbansite 0010 5212 36574 lt001
Statistically significant values forhabitat choice areboldedand indicatedifferencesbetweenutilizedandrandomlyavailablehabitat
TABLE 2emspResultsfromANCOVAsforhabitatchoicesubsequenttotheMANOVAsinTable1Degreesoffreedom(df)Fandp-value(p)aregivenforeach
df F p
Anolis cristatellus
Ambienttemperature 1216 55822 lt001
Perchtemperature 1216 0331 566
Humidity 1216 99237 lt001
Perchheight 1216 5868 016
Perchdiameter 1216 9012 003
Perchproximity 1216 23067 lt001
Vegetativecanopy 1216 4028 046
Manmadecanopy 1216 1437 232
Perchroughness 1216 1589 209
Anolis stratulus
Ambienttemperature 1212 47060 lt001
Perchtemperature 1212 29113 lt001
Humidity 1212 2660 104
Perchheight 1212 0197 658
Perchdiameter 1212 40113 lt001
Perchproximity 1212 0187 666
Vegetativecanopy 1212 319157 lt001
Manmadecanopy 1212 104938 lt001
Perchroughness 1212 238820 lt001
Shadedcellsaresignificantfordifferencebetweenuseandavailabilityatthesignificancelevelindicatedbythelastcolumn
emspensp emsp | emsp31WINCHELL Et aL
inabundancebetweenspeciesHoweverthedifferenceinabundancesmeasured inthepresentstudyfarexceedsthatfoundpreviouslyforPuertoRicanmesicforest(egRoddaetal2001)ThissuggeststhaturbanhabitatsdonotsupportA stratulusandA cristatellusinrelativeabundances proportional to those reported for more natural sitesRelative abundances in urban areas instead appear to follow a pat-ternmorecloselyresemblingnaturallyxericforests(egGenetGenetBurtonampMurphy2001)despitebeinglocatedinmesicregions
ItispossiblethatoursamplingmethodmayhavefailedtodetectA stratulus perching higher in the urban canopy Indeed in naturalhabitatsA stratulus densityhasbeenunderestimatedat somesiteswhentheyutilizecanopyhabitatForexampleReagan(1992)found
thatA stratulusattainsextremelyhighdensities(24000ndash28000ha)inforestswhereindividualsoccupyhighcanopyhabitat(approximately10ndash20mheight)Webelievethisisnotamajorconcerninourstudyasurbantreesatoursitestendedtobeshorterandrarelyproduced
F IGURE 4emspMeanandSEforhabitatvariablessampledforhabitatavailability(ldquoArdquo)andeachspeciesuse(ldquoCrdquomdashA cristatellusldquoSrdquomdashA stratulus)Differencesbetweenutilizedandavailablehabitat(summarizedinTable2)representedbygraylinesandsignificancelevelplt001plt01plt05
Ambient temp (degC)
295
300
305
310
Manmade canopy ()
10
20
Perch height (cm)
44
46
48
50
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
Perch diameter (cm)
24
27
30
33
Nearest perch (cm)
46
48
50
52
Relative humidity ()
52
54
56
58
60
290
295
300
305
Veg canop y ()
40
50
60
70
80
(log
scal
e)
Surface roughness
35
40
45
Perch temp (degC)
F IGURE 5emspClassificationtreeforhabitatusedifferencesinA cristatellusandA stratulusSpeciespercentagesindicatethepercentageofallsampledindividualsofeachspeciesineachgroup(highcanopycoverlowcanopycoverandhightemperaturelowcanopycoverandlowtemperature)
Veg canopy p lt 0001
le7404 cover gt7404 cover
Ambient tempp = 0009
le293degC gt293degC
A cristatellus 58A stratulus 149
A cristatellus 712A stratulus 8 5
A cristatellus 231A stratulus 766
TABLE 3emspResultsfromvarimax-rotatedprinciplecomponentanalysisofurbanhabitat
PC1 PC2 PC3
Humidity minus0560 0118 minus0163
Ambienttemp 0616 minus0008 0010
Perchheight minus0112 minus0040 minus0571
Perchdiameter minus0188 0477 minus0048
Nearestperch 0136 0011 minus0786
Vegcanopy minus0125 minus0631 0014
Perchtemp 0473 0108 minus0136
Perchroughness minus0042 minus0589 minus0087
Cumulativevariance 2687 5205 6528
SignificanceSpecies plt001 p = 001 p = 107
Significanceperchtype plt001 plt001 p = 002
Eigenvalue 2150 2015 1058
SignificanceforttestscomparingprincipalcomponentsbetweenA stratu-lusandA cristatellusaregivenintherowlabelledldquoSignificanceSpeciesrdquoandsignificanceforttestscomparingprincipalcomponentsbetweennatu-ralandmanmadeperchesaregivenintherowlabelledldquoSignificancePerchTyperdquoSignificantloadingsareboldedandshadedSignificancelevelsforspeciesandperchtypeANOVAsareplt001plt01
32emsp |emsp emspensp WINCHELL Et aL
dense or continuous canopy Moreover manmade substrates suchaswallsandfencesareclearlyvisibleall thewaytotherooflineAssuchvisibilityofthefewhighperchespresentwasverygoodacrossallurbansitesandwedonotexpectthatwefailedtoobserveasignif-icantnumberofindividualsathigherperches
42emsp|emspHabitat use
ThetwolizardspeciesofthisstudydifferedinthefrequencywhichtheyutilizedmanmadesubstratesasperchesAnolis cristatellususedman-madeperchesatahighfrequencybutusedbothmanmadestructuresandvegetationinproportiontotheirrelativeabundanceintheenviron-mentIncontrastA stratulusinfrequentlyoccupiedmanmadeperchesSimilarlyKolbeBattlesandAvileacutes-Rodriacuteguez(2015)foundthatA cris-tatellususedmanmadestructuresmorefrequentlythanA stratulus in human-modifiedhabitatsdespitefindingA stratulustobemoreadeptatsprintingonsmoothverticalsurfacesOurdatasuggestthatA stratu-luseitheractivelyseeksoutnaturalsubstratesoravoidstheuseofman-madesubstratesThispatternmaybeexplainedbysomecombinationofpredationcompetitionperformanceandhabitatrequirements
AtfirstglanceitappearsthatA cristatellusandA stratuluspartitionurbanniche space in similarwaysas innatural foresthabitatWhenfoundsyntopicallyinnaturalforesthabitatthesetwospeciesdividethehabitatsuchasmanyanolespeciesbasedprimarilyonstructuralandmicroclimatichabitatfeatures(Rand1964reviewedinLosos2009)InnaturalhabitatsA cristatellustypicallyusesbroaderandlowerpercheswhile A stratulususesthinnerandhigherperches(Cooper2005Rand
F IGURE 6emspPrincipalcomponents12and3plottedwith95confidenceintervalellipsesforutilizedhabitatbyeachspeciesPC1andPC2differedbetweenspeciesatsignificancelevelsplt001()andplt01()respectively
minus25
00
25
minus25 00 25 minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
A cristatellus
A stratulus
PC3
A cristatellus
A stratulus Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower perchesLess isolated perches
F IGURE 7emspPrincipalcomponents1and2plottedwith95confidenceintervalellipsesgroupedbyperchtypeforavailablehabitat(left)andutilizedhabitat(right)
Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower humidityHigher temperature (ambient amp perch)
A cristatellusManmade perches
A cristatellusNatural perches
A stratulusminus25
00
25
minus25 00 25
PC1
minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
Natural perches
Manmadeperches
TABLE 4emspResultsofANOVAandTukeyrsquosHSDcomparingprincipalcomponentsbetweenutilizedhabitatbyA stratulus(all)andA cristatellus(byperchtype)Degreesoffreedom(df)Fandp-value(p)aregivenforeachtest
ANOVA Tukeyrsquos HSD
df F p CNndashCM CNndashS CMndashS
PC1 286 24970 lt001 0313 001 lt001
PC2 286 28890 lt001 lt001 695 lt001
PC3 286 1323 272 1000 413 361
PairedcomparisonsfortheTukeyrsquosHSDtestsareA cristatellususingnatu-ralperchesversusA cristatellususingmanmadeperches(CNndashCM)A cris-tatellususingnaturalperchesversusA stratulusonallperches(CNndashS)andA cristatellus using manmade perches versus A stratulus on all perches(CMndashS)Significancelevelsplt001plt01plt05Significantre-sultsareboldedandshaded
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
emspensp emsp | emsp31WINCHELL Et aL
inabundancebetweenspeciesHoweverthedifferenceinabundancesmeasured inthepresentstudyfarexceedsthatfoundpreviouslyforPuertoRicanmesicforest(egRoddaetal2001)ThissuggeststhaturbanhabitatsdonotsupportA stratulusandA cristatellusinrelativeabundances proportional to those reported for more natural sitesRelative abundances in urban areas instead appear to follow a pat-ternmorecloselyresemblingnaturallyxericforests(egGenetGenetBurtonampMurphy2001)despitebeinglocatedinmesicregions
ItispossiblethatoursamplingmethodmayhavefailedtodetectA stratulus perching higher in the urban canopy Indeed in naturalhabitatsA stratulus densityhasbeenunderestimatedat somesiteswhentheyutilizecanopyhabitatForexampleReagan(1992)found
thatA stratulusattainsextremelyhighdensities(24000ndash28000ha)inforestswhereindividualsoccupyhighcanopyhabitat(approximately10ndash20mheight)Webelievethisisnotamajorconcerninourstudyasurbantreesatoursitestendedtobeshorterandrarelyproduced
F IGURE 4emspMeanandSEforhabitatvariablessampledforhabitatavailability(ldquoArdquo)andeachspeciesuse(ldquoCrdquomdashA cristatellusldquoSrdquomdashA stratulus)Differencesbetweenutilizedandavailablehabitat(summarizedinTable2)representedbygraylinesandsignificancelevelplt001plt01plt05
Ambient temp (degC)
295
300
305
310
Manmade canopy ()
10
20
Perch height (cm)
44
46
48
50
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
A C S
Perch diameter (cm)
24
27
30
33
Nearest perch (cm)
46
48
50
52
Relative humidity ()
52
54
56
58
60
290
295
300
305
Veg canop y ()
40
50
60
70
80
(log
scal
e)
Surface roughness
35
40
45
Perch temp (degC)
F IGURE 5emspClassificationtreeforhabitatusedifferencesinA cristatellusandA stratulusSpeciespercentagesindicatethepercentageofallsampledindividualsofeachspeciesineachgroup(highcanopycoverlowcanopycoverandhightemperaturelowcanopycoverandlowtemperature)
Veg canopy p lt 0001
le7404 cover gt7404 cover
Ambient tempp = 0009
le293degC gt293degC
A cristatellus 58A stratulus 149
A cristatellus 712A stratulus 8 5
A cristatellus 231A stratulus 766
TABLE 3emspResultsfromvarimax-rotatedprinciplecomponentanalysisofurbanhabitat
PC1 PC2 PC3
Humidity minus0560 0118 minus0163
Ambienttemp 0616 minus0008 0010
Perchheight minus0112 minus0040 minus0571
Perchdiameter minus0188 0477 minus0048
Nearestperch 0136 0011 minus0786
Vegcanopy minus0125 minus0631 0014
Perchtemp 0473 0108 minus0136
Perchroughness minus0042 minus0589 minus0087
Cumulativevariance 2687 5205 6528
SignificanceSpecies plt001 p = 001 p = 107
Significanceperchtype plt001 plt001 p = 002
Eigenvalue 2150 2015 1058
SignificanceforttestscomparingprincipalcomponentsbetweenA stratu-lusandA cristatellusaregivenintherowlabelledldquoSignificanceSpeciesrdquoandsignificanceforttestscomparingprincipalcomponentsbetweennatu-ralandmanmadeperchesaregivenintherowlabelledldquoSignificancePerchTyperdquoSignificantloadingsareboldedandshadedSignificancelevelsforspeciesandperchtypeANOVAsareplt001plt01
32emsp |emsp emspensp WINCHELL Et aL
dense or continuous canopy Moreover manmade substrates suchaswallsandfencesareclearlyvisibleall thewaytotherooflineAssuchvisibilityofthefewhighperchespresentwasverygoodacrossallurbansitesandwedonotexpectthatwefailedtoobserveasignif-icantnumberofindividualsathigherperches
42emsp|emspHabitat use
ThetwolizardspeciesofthisstudydifferedinthefrequencywhichtheyutilizedmanmadesubstratesasperchesAnolis cristatellususedman-madeperchesatahighfrequencybutusedbothmanmadestructuresandvegetationinproportiontotheirrelativeabundanceintheenviron-mentIncontrastA stratulusinfrequentlyoccupiedmanmadeperchesSimilarlyKolbeBattlesandAvileacutes-Rodriacuteguez(2015)foundthatA cris-tatellususedmanmadestructuresmorefrequentlythanA stratulus in human-modifiedhabitatsdespitefindingA stratulustobemoreadeptatsprintingonsmoothverticalsurfacesOurdatasuggestthatA stratu-luseitheractivelyseeksoutnaturalsubstratesoravoidstheuseofman-madesubstratesThispatternmaybeexplainedbysomecombinationofpredationcompetitionperformanceandhabitatrequirements
AtfirstglanceitappearsthatA cristatellusandA stratuluspartitionurbanniche space in similarwaysas innatural foresthabitatWhenfoundsyntopicallyinnaturalforesthabitatthesetwospeciesdividethehabitatsuchasmanyanolespeciesbasedprimarilyonstructuralandmicroclimatichabitatfeatures(Rand1964reviewedinLosos2009)InnaturalhabitatsA cristatellustypicallyusesbroaderandlowerpercheswhile A stratulususesthinnerandhigherperches(Cooper2005Rand
F IGURE 6emspPrincipalcomponents12and3plottedwith95confidenceintervalellipsesforutilizedhabitatbyeachspeciesPC1andPC2differedbetweenspeciesatsignificancelevelsplt001()andplt01()respectively
minus25
00
25
minus25 00 25 minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
A cristatellus
A stratulus
PC3
A cristatellus
A stratulus Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower perchesLess isolated perches
F IGURE 7emspPrincipalcomponents1and2plottedwith95confidenceintervalellipsesgroupedbyperchtypeforavailablehabitat(left)andutilizedhabitat(right)
Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower humidityHigher temperature (ambient amp perch)
A cristatellusManmade perches
A cristatellusNatural perches
A stratulusminus25
00
25
minus25 00 25
PC1
minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
Natural perches
Manmadeperches
TABLE 4emspResultsofANOVAandTukeyrsquosHSDcomparingprincipalcomponentsbetweenutilizedhabitatbyA stratulus(all)andA cristatellus(byperchtype)Degreesoffreedom(df)Fandp-value(p)aregivenforeachtest
ANOVA Tukeyrsquos HSD
df F p CNndashCM CNndashS CMndashS
PC1 286 24970 lt001 0313 001 lt001
PC2 286 28890 lt001 lt001 695 lt001
PC3 286 1323 272 1000 413 361
PairedcomparisonsfortheTukeyrsquosHSDtestsareA cristatellususingnatu-ralperchesversusA cristatellususingmanmadeperches(CNndashCM)A cris-tatellususingnaturalperchesversusA stratulusonallperches(CNndashS)andA cristatellus using manmade perches versus A stratulus on all perches(CMndashS)Significancelevelsplt001plt01plt05Significantre-sultsareboldedandshaded
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
32emsp |emsp emspensp WINCHELL Et aL
dense or continuous canopy Moreover manmade substrates suchaswallsandfencesareclearlyvisibleall thewaytotherooflineAssuchvisibilityofthefewhighperchespresentwasverygoodacrossallurbansitesandwedonotexpectthatwefailedtoobserveasignif-icantnumberofindividualsathigherperches
42emsp|emspHabitat use
ThetwolizardspeciesofthisstudydifferedinthefrequencywhichtheyutilizedmanmadesubstratesasperchesAnolis cristatellususedman-madeperchesatahighfrequencybutusedbothmanmadestructuresandvegetationinproportiontotheirrelativeabundanceintheenviron-mentIncontrastA stratulusinfrequentlyoccupiedmanmadeperchesSimilarlyKolbeBattlesandAvileacutes-Rodriacuteguez(2015)foundthatA cris-tatellususedmanmadestructuresmorefrequentlythanA stratulus in human-modifiedhabitatsdespitefindingA stratulustobemoreadeptatsprintingonsmoothverticalsurfacesOurdatasuggestthatA stratu-luseitheractivelyseeksoutnaturalsubstratesoravoidstheuseofman-madesubstratesThispatternmaybeexplainedbysomecombinationofpredationcompetitionperformanceandhabitatrequirements
AtfirstglanceitappearsthatA cristatellusandA stratuluspartitionurbanniche space in similarwaysas innatural foresthabitatWhenfoundsyntopicallyinnaturalforesthabitatthesetwospeciesdividethehabitatsuchasmanyanolespeciesbasedprimarilyonstructuralandmicroclimatichabitatfeatures(Rand1964reviewedinLosos2009)InnaturalhabitatsA cristatellustypicallyusesbroaderandlowerpercheswhile A stratulususesthinnerandhigherperches(Cooper2005Rand
F IGURE 6emspPrincipalcomponents12and3plottedwith95confidenceintervalellipsesforutilizedhabitatbyeachspeciesPC1andPC2differedbetweenspeciesatsignificancelevelsplt001()andplt01()respectively
minus25
00
25
minus25 00 25 minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
A cristatellus
A stratulus
PC3
A cristatellus
A stratulus Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower perchesLess isolated perches
F IGURE 7emspPrincipalcomponents1and2plottedwith95confidenceintervalellipsesgroupedbyperchtypeforavailablehabitat(left)andutilizedhabitat(right)
Sm
ooth
er amp
bro
ader
per
ches
Less
can
opy
cove
r
Lower humidityHigher temperature (ambient amp perch)
A cristatellusManmade perches
A cristatellusNatural perches
A stratulusminus25
00
25
minus25 00 25
PC1
minus25 00 25
PC1
PC
2
Lower humidityHigher temperature (ambient amp perch)
Natural perches
Manmadeperches
TABLE 4emspResultsofANOVAandTukeyrsquosHSDcomparingprincipalcomponentsbetweenutilizedhabitatbyA stratulus(all)andA cristatellus(byperchtype)Degreesoffreedom(df)Fandp-value(p)aregivenforeachtest
ANOVA Tukeyrsquos HSD
df F p CNndashCM CNndashS CMndashS
PC1 286 24970 lt001 0313 001 lt001
PC2 286 28890 lt001 lt001 695 lt001
PC3 286 1323 272 1000 413 361
PairedcomparisonsfortheTukeyrsquosHSDtestsareA cristatellususingnatu-ralperchesversusA cristatellususingmanmadeperches(CNndashCM)A cris-tatellususingnaturalperchesversusA stratulusonallperches(CNndashS)andA cristatellus using manmade perches versus A stratulus on all perches(CMndashS)Significancelevelsplt001plt01plt05Significantre-sultsareboldedandshaded
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
emspensp emsp | emsp33WINCHELL Et aL
1964Reagan1992)Thecomplexityofthepercheschosenalsodif-ferswithA cristatellususingrelativelysimplerlessbranchingperchescomparedtoA stratulus(PowellampLeal2014)Intermsofclimatichab-itatinnaturalareasA cristatellustypicallyusesperchesthatarehigherintemperatureandlowerinhumidityoftenwithreducedtreecovercomparedtothoseusedbyA stratulus(Cooper2006HeatwoleLinVillaloacutenMuntildeizampMatta1969Rand1964)
Inurbanhabitatswefoundthatthetwospeciesselectstructuralhabitat based on similar factors In particularwe found thatA cri-statellusutilizedbroadandlowpercheswhileA stratulusutilizedthinandhighperchesReagan (1992) foundhigherperchesalso tend tobethinnerandconcludedthatperchdiameternotheightmaybethedrivingfactorindeterminingstructuralhabitatuseinA stratulusper-hapsbecauselargerpredatoryspeciescannotlocomoteeffectivelyonthinnerperches InadditionA stratulus is thought tomorestronglyrelyoncrypsistoavoidpredationwhileA cristatellusmoreoftenfleesfrompotentialpredators(Cooper2006Heatwole1968)IfA strat-ulus experiences elevated predation on substrateswhere it ismoreexposedor if it isunabletocompetewiththe largerandpredatoryA cristatellusonthesesubstratesitmayavoidthishabitattypeThesefactorscouldhelpexplainthepatternofhabitatusethatweobservedinurbansettings Inparticular themajorityofmanmadeperches inurban areas are broad and simple (ie non-branching) and differ inpatternandcolorcomparedtonaturalsubstratesThusthesesurfacesoffer relatively fewrefuges littleopportunity toavoidpredatorsviacrypsisandnolocomotoradvantagesforspeciesadaptedtothinnerperchessuchasA stratulus
Wealso found thatboth species segregateurbanhabitat basedonmicroclimaticvariablessimilar to those innaturalhabitatsAnolis cristatellusselectedpercheswithhighertemperaturelowerhumidityandrelativelylittlecanopycoverwhileA stratuluschosepercheswithlowersurfaceandairtemperaturesandmoreextensivecanopycoverDifferencesinthermalpreferencesmaybekeytounderstandingboththelowerabundancesandpreferenceforheavilyshadednaturalsub-strates thatwe show forA stratulus Specifically the microclimaticfactorsonwhichthisspeciesdiscriminatelychoosesperchesaresim-plylesscommoninurbanenvironmentsTheurbanhabitattendstobehotteranddrierdueto increased impervioussurfaceanddecreasedcanopycoverandmanmadesubstrateshavedifferentthermalproper-tiescomparedtonaturalsurfaces(Forman2014)StudiesfromnaturalforesthabitatssuggestthatthesespeciesdifferinthermalphysiologyForexample juvenileA stratulus inxericforestsaresensitivetolowhumidityandhightemperatureconditions(Nicholsonetal2005)andadultA cristatellusfrombothlowlandanduplandmesicforestspreferwarmertemperaturesandcantoleratehighertemperaturescomparedtoA stratulus (Heatwoleetal1969)Anolis stratulusmaysimplybetooconstrainedtotoleratethephysiologicalstressesassociatedwiththemostintenselybuiltcomponentsofurbanhabitats
43emsp|emspNiche partitioning
Our classification tree analysis indicates that two environmentalfactors in particular aremost important in determining habitat use
vegetativecanopycoverandambienttemperatureatperchsitesThemajorityofA stratulusoccupiedpercheswithextremelyhighcanopycoverandthefewthatdidnotchoosesiteswithrelativelylowambi-enttemperaturesIncontrastthemajorityofA cristatellusoccupiedsiteswithbothlowcanopycoverandhighambienttemperaturesThisindicates that thermalpreferencesand tolerancesare likelyamajorfactorindetermininghabitatuseinurbanareasInterestinglyA strat-ulusinthisstudychoseperchesthathadhighvegetativecanopycoverbutlowmanmadecanopycoverThissuggeststhatsomefactorcorre-latedwithvegetativecanopycover(andnotsimplytheloweredtem-peraturesofferedbyshade)maybeimportantinhabitatuseforthisspecies perhaps related to associatedprey insectsormicroclimaticconditions
ThepatternsofhabitatuseandavailabilitypaintaninterestingpictureofhabitatpartitioningintheurbanenvironmentBothspe-ciesdemonstratenonrandomhabitatselectionfordifferentaspectsoftheirstructuralandmicroclimaticenvironmentsOuranalysisofprincipal components shows that both structural and climatic at-tributes of the perch are significant in describing habitat use dif-ferencesOverallA cristatelluswasmoregeneralizedinitshabitatusewhileA stratuluswas highly selective using a subset of bothtotal available habitat andof the habitat utilized byA cristatellus Interestingly although no explicitly urban habitat variables wereincluded in the principal component analysis the habitat spaceuniquelyoccupiedbyA cristatelluswasassociatedwithcharacteris-ticsofmoreintenseurbanization lowerhumidityhighertempera-tures smoother and broader perches and decreased vegetativecanopy coverUse of this urban-associated habitat space reducesnicheoverlapwithA stratuluswhichismainlyrestrictedtohabitatassociatedwithnaturalperchesWhetherthisrepresentsaprefer-ence for anthropogenic habitat byA cristatellus or simply a toler-anceofthisabundanthabitattypeinurbanareasisnotaquestionwecananswerwithourcurrentdatasetbutisonethatwehopetofurtherexploreinongoingresearch
Inconclusionwehaveshownthattwocommonspeciesofanolesthatobtainhighabundancesinsympatryinnaturalhabitatshaveverydifferent responses to urbanization in terms of relative abundanceandhabitatuseThedifferentialuseofurbanhabitat in somewaysreflects patterns observed in natural habitats in terms of structuralandmicroclimatichabitat but alsodemonstrates that these speciesare utilizing anthropogenic resources specifically habitat associatedwithmanmadeperches todifferingdegreesWefind thatA stratu-lus is restricted tonatural habitat elementswithin theurbanmatrixwhile A cristatellus exploits novel habitat associatedwithmanmadestructuresThisdivisionoftheurbanhabitatresultsindecreasednicheoverlapassociatedwithtwodistinctnichespacesnaturalandman-madesubstratesThisprovidesempiricalevidenceforthehypothesisthatsomespeciesareurbanophilicwhileothersaremerelytolerantofurbanization
TheCaribbeanislandshaveexperiencedurbanizationpressuresforoverfivecenturiesyettheimplicationsofthishabitatmodificationareonlynowbeingstudied(egAckleyMuellemanCarterHendersonampPowell2009GermanoSanderHendersonampPowell2003Mallery
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
34emsp |emsp emspensp WINCHELL Et aL
MarcumPowellParmerleeampHenderson2003MarnochaPollingerampSmith2011Winchelletal2016)Understandingthefactorsofurban-izationtowhichspeciesareabletoadaptiscriticaltosuccessfulcon-servationmanagement inurbanhabitats (DonihueampLambert2015)Ourfindingsreinforcetheideathatunderstandingspeciesrsquonaturalhis-toryparticularlydifferences inhabitatuse isan importantprecursorto understanding how specieswill respond to intensifying urbaniza-tionincomingyearsBroadhabitatpreferencesandahighfrequencyofutilizationofurban resourcesasweobserved inA cristatellus setthestageforevolutionaryadaptationtourbanenvironmentalchangeinurbanophilicspecies(egWinchelletal2016)Bycontrastapparentavoidanceofurbansubstratesandahighfrequencyofutilizationoftheremnantnatural resourcesasweobserved inA stratulus remindsusnottoexpectthatallurban-tolerantspecieswillbeequallyresistanttolocalextirpationwithincreasinglyintenseurbandevelopment
ACKNOWLEDGEMENTS
WethankUniversityofPuertoRico inAreciboand InteramericanUniversity inArecibo for allowing us to conduct this research ontheircampusesWethankJLi forassistance inthefieldandthefollowingpeople foradvice inplanningandconducting thestudyS Vega-Castillo J KolbeDMuntildeizWe also thank the followingpeopleforprovidingvaluablefeedbackonthismanuscriptJLososCDonihueAKamathO LaPiedraAGeneva PMuralidhar SPrado-Irwinandthemanypeoplewhoofferedconstructivecom-ments at the JointMeeting of Ichthyologists andHerpetologistsThis study was conducted under Permit 2014-IC-024 (O-VS-PVS15-SJ-00375-22042014) from thePuertoRicoDepartamentode Recursos Naturales y Ambientales (DRNA) This research wasfunded by a grant from the National Science Foundation to LJR(DEB1354044)
CONFLICT OF INTEREST
Nonedelcared
AUTHOR CONTRIBUTIONS
KMW and LJR conceived the project and designed methodologyKMWARPRandLJRidentifiedstudylocationsandsecuredsiteper-missionsKMWandEJCcollectedthedataKMWandLJRanalyzedthedatawith input fromARPRandEJCAll authors contributed tothewritingofthemanuscriptandgavefinalapprovalforpublication
DATA ACCESSIBILITY
Data are available on Dryad Digital Repository (httpsdoiorg105061dryad6fq63)
ORCID
Kristin M Winchell httporcidorg0000-0002-5217-4809
REFERENCES
AckleyJWMuellemanPJCarterREHendersonRWampPowellR (2009)A rapid assessmentofherpetofaunaldiversity invariouslyalteredhabitatsonDominicaApplied Herpetology6171ndash184httpsdoiorg101163157075408X394124
AronsonMFJ LaSorteFANilonCHKattiMGoddardMALepczykCAhellipWinterM (2014)Aglobalanalysisof the impactsofurbanizationonbirdandplantdiversityrevealskeyanthropogenicdriversProceedings of the Royal Society B28120133330httpsdoiorg101098rspb20133330
CartmillM(1985)ClimbingInMHildebrandDMBrambleKFLiemamp D B Wake (Eds) Functional vertebrate morphology (pp 73ndash88)CambridgeMABelknap
CooperWEJr(2005)EcomorphologicalvariationinforagingbehaviourbyPuertoRicanAnolislizardsJournal of Zoology265133ndash139httpsdoiorg101017S0952836904006065
CooperWEJr(2006)RiskfactorsaffectingescapebehaviourbyPuertoRicanAnolislizardsCanadian Journal of Zoology84495ndash504httpsdoiorg101139z06-018
Donihue C M amp Lambert M R (2015) Adaptive evolution in urbanecosystems Ambio 44 194ndash203 httpsdoiorg101007s13280-014-0547-2
Forman R T T (2014)Urban ecology Science of cities Cambridge UKCambridgeUniversityPress
GenetKSGenetJABurtonTMampMurphyPG (2001)The liz-ardcommunityofasubtropicaldryforestGuaacutenicaforestPuertoRicoTropical Ecology4297ndash109
Germano J M Sander J M Henderson R W amp Powell R (2003)HerpetofaunalcommunitiesinGrenadaAcomparisonofalteredsiteswith an annotated checklist of Grenadian amphibians and reptilesCaribbean Journal of Science3968ndash76
Grant BWMiddendorf G ColganM JAhmad H ampVogelM B(2011) Ecology of urban amphibians and reptiles Urbanophiles ur-banophobes and theurbanoblivious InJNiemela (Ed)Urban ecol-ogy (pp 167ndash178)OxfordUKOxfordUniversity Press httpsdoiorg101093acprofoso97801995635620010001
HarrisSEMunshi-SouthJObergfellCampOrsquoNeillR(2013)Signaturesof rapidevolution inurbanand rural transcriptomesofwhite-footedmice (Peromyscus leucopus) in theNewYorkmetropolitan areaPLoS ONE8e74938httpsdoiorg101371journalpone0074938
Heatwole H (1968) Relationship of escape behavior and cam-ouflage in Anoline lizards Copeia 1 109ndash113 httpsdoiorg1023071441557
HeatwoleHLinTVillaloacutenEMuntildeizAampMattaA(1969)Someas-pects of the thermal ecology of the Puerto Rican Anoline lizardsJournal of Herpetology365ndash77httpsdoiorg1023071563225
Helmer E H (2004) Forest conservation and land development inPuerto Rico Landscape Ecology19 29ndash40 httpsdoiorg101023BLAND000001836468514fb
HendersonRWampPowellR(2001)ResponsesbytheWestIndianher-petofaunatohuman-influencedresourcesCaribbean Journal of Science3741ndash54
HertzPE (1992)EvaluatingthermalresourcepartitioningbysympatriclizardsAnolis cookiandAnolis cristatellusAfieldtestusingnullhypoth-esesOecologia90127ndash136httpsdoiorg101007BF00317818
HothornTHornikKampZeileisA(2006)UnbiasedrecursivepartitioningAconditionalinferenceframeworkJournal of Computational and Graphical Statistics15651ndash674httpsdoiorg101198106186006X133933
Koenig N (1953) A comprehensive agricultural program for Puerto Rico Washington DC USA US Department of Agriculture andCommonwealthofPuertoRico
KolbeJJBattlesACampAvileacutes-RodriacuteguezKJ (2015)CityslickersPoor performance does not deterAnolis lizards fromusing artificialsubstratesinhuman-modifiedhabitatsFunctional Ecology301418ndash1429httpsdoiorg1011111365-243512607
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
RCoreDevelopmentTeam(2012)R A language and environment for statisti-cal computingViennaAustriaRFoundationforStatisticalComputing
RandAS(1964)EcologicaldistributioninAnolinelizardsofPuertoRicoEcology45745ndash752httpsdoiorg1023071934922
ReaganD P (1992) Congeneric species distribution and abundance ina three-dimensional habitat The rain forest anoles of Puerto RicoCopeia1992(2)392ndash403httpsdoiorg1023071446199
RoddaGHPerryGRondeauRJampLazellJ(2001)Thedensestter-restrialvertebrateJournal of Tropical Ecology17331ndash338httpsdoiorg101017S0266467401001225
Shochat E Lerman SBAnderies JMWarren P S Faeth SHampNilon C H (2010) Invasion competition and biodiversity loss inurbanecosystemsBioScience60199ndash208httpsdoiorg101525bio20106036
ShochatEWarrenPSFaethSHMcIntyreNEampHopeD(2006)From patterns to emerging processes inmechanistic urban ecologyTrends in Ecology and Evolution21186ndash191httpsdoiorg101016jtree200511019
United Nations (2012)World Urbanization Prospects the 2011 Revision Final Report with Annex TablesUnitedNationsDepartmentofEconomicandSocialAffairsPopulationDivisionNewYorkNY
US Census Bureau (2012) 2010 Census of Population and Housing Summary Population and Housing Characteristics CPH-1-53 Puerto Rico USGovernmentPrintingOfficeWashingtonDCUSA
WinchellKMReynoldsRGPrado-IrwinSRPuente-RoloacutenARampRevellLJ(2016)PhenotypicshiftsinurbanareasinthetropicallizardAnolis cristatellus Evolution701009ndash1022httpsdoiorg101111evo201670issue-5
SUPPORTING INFORMATION
Additional Supporting Information may be found online in thesupportinginformationtabforthisarticle
How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
emspensp emsp | emsp35WINCHELL Et aL
LoacutepezTMAideTMampThomlinsonJR(2001)UrbanexpansionandthelossofprimeagriculturallandsinPuertoRicoAmbio3049ndash54httpsdoiorg1015790044-7447-30149
LososJB(2009)Lizards in an evolutionary tree Ecology and adaptive radia-tion of anolesBerkeleyCAUniversityofCaliforniaPress
MalleryCSMarcumMAPowellRParmerleeJ SampHendersonR W (2003) Herpetofaunal communities of the leeward slopesand coasts of St Vincent A comparison of sites variously alteredby human activity Applied Herpetology 4 313ndash325 httpsdoiorg101163157075407782424494
MarnochaEPollingerJampSmithTB(2011)Human-inducedmorpho-logicalshiftsinanislandlizardEvolutionary Applications4388ndash396httpsdoiorg101111j1752-4571201000170x
MartinuzziSGouldWAampRamosGonzaacutelezOM(2007)Landdevel-opmentlanduseandurbansprawlinPuertoRicointegratingremotesensingandpopulationcensusdataLandscape and Urban Planning79288ndash297httpsdoiorg101016jlandurbplan200602014
McKinney M L (2002) Urbanization biodiversity and con-servation BioScience 52 883ndash890 httpsdoiorg1016410006-3568(2002)052[0883UBAC]20CO2
McKinney M L (2006) Urbanization as a major cause of biotic ho-mogenization Biological Conservation 127 247ndash260 httpsdoiorg101016jbiocon200509005
McKinneyML(2008)EffectsofurbanizationonspeciesrichnessAre-viewofplantsandanimalsUrban Ecosystems11161ndash176httpsdoiorg101007s11252-007-0045-4
MillerGLampLugoAE(2009)Guide to the ecological systems of Puerto Rico General Technical Report IITF-GTR-35 US Department ofAgricultureForestServiceInternationalInstituteofTropicalForestrySanJuanPuertoRicoUSA
NicholsonKLTorrenceSMGhiocaDMBhattacharjeeJAndreiAEOwenJhellipPerryG(2005)TheinfluenceoftemperatureandhumidityonactivitypatternsofthelizardsAnolis stratulusandAmeiva exsul in the British Virgin Islands Caribbean Journal of Science 41870ndash873
PerryGBuchananBWFisherRNSalmonMampWiseSE(2008)Effectsofartificialnight lightingonamphibiansandreptiles inurbanenvironments InJCMitchellREJungBrownampBBartholomew(Eds)Urban herpetology(pp239ndash256)SaltLakeCityUTSocietyfortheStudyofAmphibiansandReptiles
PowellBJampLealM(2014)Brainorganizationandhabitatcomplexityin Anolis lizardsBrain Behavior and Evolution84 8ndash18 httpsdoiorg101159000362197
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How to cite this articleWinchellKMCarlenEJPuente- RoloacutenARRevellLJDivergenthabitatuseoftwourbanlizardspeciesEcol Evol 2018825ndash35 httpsdoiorg101002ece33600
