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Evolutionary Applications. 2018;1–15. | 1 wileyonlinelibrary.com/journal/eva Received: 15 May 2018 | Revised: 1 October 2018 | Accepted: 2 October 2018 DOI: 10.1111/eva.12721 SPECIAL ISSUE ORIGINAL ARTICLE Urbanization erodes niche segregation in Darwin's finches Luis F. De León 1,2 | Diana M. T. Sharpe 3 | Kiyoko M. Gotanda 3,4 | Joost A. M. Raeymaekers 5,6 | Jaime A. Chaves 7,8 | Andrew P. Hendry 3 | Jeffrey Podos 9 1 Department of Biology, University of Massachusetts Boston, Boston, Massachusetts 2 Centro de Biodiversidad y Descubrimiento de Drogas, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología (INDICASAT‐AIP), Panamá City, Panamá 3 Redpath Museum, Department of Biology, McGill University, Montréal, Quebec, Canada 4 Department of Zoology, University of Cambridge, Cambridge, UK 5 Centre for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway 6 Laboratory of Biodiversity and Evolutionary Genomics, University of Leuven, Leuven, Belgium 7 Colegio de Ciencias Biológicas y Ambientales, Universidad San Francisco de Quito, Diego de Robles y Pampite, Quito, Ecuador 8 Galápagos Science Center, Puerto Baquerizo Moreno, Galápagos, Ecuador 9 Department of Biology, University of Massachusetts Amherst, Amherst, Massachusetts 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. © 2018 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd Correspondence Luis F. De León, Department of Biology, University of Massachusetts Boston. Boston, MA. Email: [email protected] Funding information Earthwatch Institute; Secretaría Nacional de Ciencia, Tecnología e Innovación; Sigma Xi; McGill University; University of Massachusetts Boston; National Science and Engineering Research Council of Canada Vanier Scholarship; European Society for Evolutionary Biology; GAIAS‐USFQ; Sistema Nacional de Investigación Abstract Urbanization is influencing patterns of biological evolution in ways that are only be‐ ginning to be explored. One potential effect of urbanization is in modifying ecological resource distributions that underlie niche differences and that thus promote and maintain species diversification. Few studies have assessed such modifications, or their potential evolutionary consequences, in the context of ongoing adaptive radia‐ tion. We study this effect in Darwin’s finches on the Galápagos Islands, by quantify‐ ing feeding preferences and diet niche partitioning across sites with different degrees of urbanization. We found higher finch density in urban sites and that feeding prefer‐ ences and diets at urban sites skew heavily toward human food items. Furthermore, we show that finches at urban sites appear to be accustomed to the presence of people, compared with birds at sites with few people. In addition, we found that human behavior via the tendency to feed birds at non‐urban but tourist sites is likely an important driver of finch preferences for human foods. Site differences in diet and feeding behavior have resulted in larger niche breadth within finch species and wider niche overlap between species at the urban sites. Both factors effectively minimize niche differences that would otherwise facilitate interspecies coexistence. These findings suggest that both human behavior and ongoing urbanization in Galápagos are starting to erode ecological differences that promote and maintain adaptive ra‐ diation in Darwin’s finches. Smoothing of adaptive landscapes underlying diversifica‐ tion represents a potentially important yet underappreciated consequence of

SPECIAL ISSUE ORIGINAL ARTICLE³n...SPECIAL ISSUE ORIGINAL ARTICLE Urbanization erodes niche segregation in Darwin's finches Luis F. De León1,2 | Diana M. T. Sharpe3 | Kiyoko M. Gotanda3,4

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  • Evolutionary Applications. 2018;1–15.  | 1wileyonlinelibrary.com/journal/eva

    Received:15May2018  |  Revised:1October2018  |  Accepted:2October2018DOI:10.1111/eva.12721

    S P E C I A L I S S U E O R I G I N A L A R T I C L E

    Urbanization erodes niche segregation in Darwin's finches

    Luis F. De León1,2  | Diana M. T. Sharpe3 | Kiyoko M. Gotanda3,4 |  Joost A. M. Raeymaekers5,6 | Jaime A. Chaves7,8 | Andrew P. Hendry3 | Jeffrey Podos9

    1DepartmentofBiology,UniversityofMassachusettsBoston,Boston,Massachusetts2CentrodeBiodiversidadyDescubrimientodeDrogas,InstitutodeInvestigacionesCientíficasyServiciosdeAltaTecnología(INDICASAT‐AIP),PanamáCity,Panamá3RedpathMuseum,DepartmentofBiology,McGillUniversity,Montréal,Quebec,Canada4DepartmentofZoology,UniversityofCambridge,Cambridge,UK5CentreforBiodiversityDynamics,DepartmentofBiology,NorwegianUniversityofScienceandTechnology,Trondheim,Norway6LaboratoryofBiodiversityandEvolutionaryGenomics,UniversityofLeuven,Leuven,Belgium7ColegiodeCienciasBiológicasyAmbientales,UniversidadSanFranciscodeQuito,DiegodeRoblesyPampite,Quito,Ecuador8GalápagosScienceCenter,PuertoBaquerizoMoreno,Galápagos,Ecuador9DepartmentofBiology,UniversityofMassachusettsAmherst,Amherst,Massachusetts

    ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,providedtheoriginalworkisproperlycited.©2018TheAuthors.Evolutionary ApplicationspublishedbyJohnWiley&SonsLtd

    CorrespondenceLuisF.DeLeón,DepartmentofBiology,UniversityofMassachusettsBoston.Boston,MA.Email:[email protected]

    Funding informationEarthwatchInstitute;SecretaríaNacionaldeCiencia,TecnologíaeInnovación;SigmaXi;McGillUniversity;UniversityofMassachusettsBoston;NationalScienceandEngineeringResearchCouncilofCanadaVanierScholarship;EuropeanSocietyforEvolutionaryBiology;GAIAS‐USFQ;SistemaNacionaldeInvestigación

    AbstractUrbanizationisinfluencingpatternsofbiologicalevolutioninwaysthatareonlybe‐ginningtobeexplored.Onepotentialeffectofurbanizationisinmodifyingecologicalresource distributions that underlie niche differences and that thus promote andmaintainspeciesdiversification.Fewstudieshaveassessedsuchmodifications,ortheirpotentialevolutionaryconsequences,inthecontextofongoingadaptiveradia‐tion.WestudythiseffectinDarwin’sfinchesontheGalápagosIslands,byquantify‐ingfeedingpreferencesanddietnichepartitioningacrosssiteswithdifferentdegreesofurbanization.Wefoundhigherfinchdensityinurbansitesandthatfeedingprefer‐encesanddietsaturbansitesskewheavilytowardhumanfooditems.Furthermore,we show that finches aturban sites appear tobeaccustomed to thepresenceofpeople, comparedwith birds at siteswith fewpeople. In addition,we found thathumanbehaviorviathetendencytofeedbirdsatnon‐urbanbuttouristsitesislikelyanimportantdriveroffinchpreferencesforhumanfoods.Sitedifferencesindietandfeedingbehaviorhaveresultedinlargernichebreadthwithinfinchspeciesandwidernicheoverlapbetweenspeciesattheurbansites.Bothfactorseffectivelyminimizeniche differences that would otherwise facilitate interspecies coexistence. ThesefindingssuggestthatbothhumanbehaviorandongoingurbanizationinGalápagosarestartingtoerodeecologicaldifferencesthatpromoteandmaintainadaptivera‐diationinDarwin’sfinches.Smoothingofadaptivelandscapesunderlyingdiversifica‐tion represents a potentially important yet underappreciated consequence of

    www.wileyonlinelibrary.com/journal/evamailto:http://orcid.org/0000-0001-9317-420Xhttp://creativecommons.org/licenses/by/4.0/mailto:[email protected]://crossmark.crossref.org/dialog/?doi=10.1111%2Feva.12721&domain=pdf&date_stamp=2018-12-18

  • 2  |     DE LEÓN Et aL.

    1  | INTRODUC TION

    One of the hallmarks of adaptive radiation is niche segregation,wherebycloselyrelatedpopulationsorspeciesevolvetospecializeondistinctecologicalresources(Grant,1999;Lack,1947;Schluter,2000;Simpson,1953).Nichesegregationisthoughttoemergeprin‐cipally from competition for shared ecological resources (Gause,1934;Hardin,1960;Macarthur&Levins,1967;Roughgarden,1976;Schoener,1968)andisdeterminedjointlybytheavailabilityofeco‐logicalresourcesandtheabilityofconsumerpopulationstoexploitthose resources. Accordingly, variation in resource distributionscan facilitatenichesegregationbetweenpopulationsorspecies ina given environment (De León, Podos,Gardezi,Herrel,&Hendry,2014; Levine & HilleRisLambers, 2009; Pianka, 1973; Schoener,1974;Tilman,1982).Nichesegregationcanalsobefavoredbyaddi‐tionalfactors,includingbehavioralflexibilityorphenotypicplasticity,wherebyindividualsexplorenovelresourceswithinsharedenviron‐ments (Boogert, Monceau, & Lefebvre, 2010; Ducatez, Clavel, &Lefebvre, 2015; Inouye, 1978;Nicolakakis, Sol,& Lefebvre, 2003;Sol,González‐Lagos,Moreira,Maspons,&Lapiedra,2014;Wright,Eberhard,Hobson,Avery,&Russello,2010)orbygeneticallybasedphenotypicvariability,wherebyindividualswithdifferenttraitvaluesexploitanddiverge intoresourcestowhichtheyarebestadapted(Bolnick&Paull,2009;Bolnick,Svanbäck,Araújo,&Persson,2007;DeLeón,Rolshausen,Bermingham,Podos,&Hendry,2012).

    Theprocessofdivergencevianichesegregationcanbecon‐ceptualized as the splitting of populations along a “rugged”adaptivelandscape—asurfacerelatingthemeanfitnessofpopu‐lationsorspeciestomeantraitvalues,with“ruggedness”arisingfromdistinctalternative fitnesspeaks thatcorrespondtodiffer‐ent ecological resources (Simpson, 1953; Svensson & Calsbeek,2012). As such, alterations to resource availability and resourcedistributionsareviewedasaffectingtheshapeofadaptive land‐scapes underlying diversification (De León et al., 2011; Hendryet al., 2006). Alterations to adaptive landscapes can be partic‐ularly drastic in the case of human disturbances such as urban‐ization, where large swathes of natural environments—and theresources they contain—are altered by many factors, includinginfrastructure development, the introduction of exotic species,andhumanfoodavailability (Alberti,2015;Aronsonetal.,2014;Gaston, 2010; Gotanda, Hendry, & Svensson, 2017; McKinney,2002, 2006 ; Penick, Savage, & Dunn, 2015). However, despitethe rapid increase in urbanization worldwide (Grimm et al.,

    2008; Seto, Sánchez‐Rodríguez, & Fragkias, 2010; Wigginton,Fahrenkamp‐Uppenbrink,Wible,&Malakoff,2016),andaccumu‐latingevidencethatsomespeciescanadaptaccordingly(Donihue& Lambert, 2014; Johnson & Munshi‐South, 2017; Kettlewell,1955;Littleford‐Colquhoun,Clemente,Whiting,Ortiz‐Barrientos,& Frère, 2017; Lowry, Lill, &Wong, 2013; Slabbekoorn & Peet,2003;Winchell, Reynolds, Prado‐Irwin, Puente‐Rolón, & Revell,2016),theexploitationofhuman‐introducedecologicalresourceshas not yet been linked to the alteration of specific ecologicalnichesoradaptivelandscapesthatdrivediversificationinnature.Here,weexploresuchlinksinDarwin’sgroundfinches(Geospiza spp.)acrosssiteswithdifferentdegreesofurbanizationonSantaCruzIsland,Galápagos,Ecuador.Specifically,weaskthefollowing:(a)Hastheavailabilityofnovelhumanfoodsinurbanareasalteredfinchdiets?;and,ifso,(b)Dofinchesinurbanenvironmentspreferhumanfoodsovernaturalfoods?;(c)Dofinchesinurbanareasre‐sponddifferentlytothepresenceofpeople?;and(d)Whataretheconsequencesoffinches’useofhumanfoodsforthepersistenceofecologicaldifferencesunderlyingthefinchadaptiveradiation?

    IntheadaptiveradiationofDarwin’sfinches,beakmorphologyhasdiversifiedasaconsequenceofadaptationtodifferentecolog‐icalresources.Forinstance,inthegroundfinches,divergentbeaksizes and shapes are considered adaptations to exploit differentseedtypes(SupportingInformationFigureS1),presumablycorre‐sponding todifferentpeakson theiradaptive landscape (Abbott,Abbott,&Grant,1977;Bowman,1961;Grant&Grant,2008;Lack,1947;Schluter&Grant,1984).Specifically,thesmall,medium,andlargegroundfinches(Geospiza fuliginosa, G. fortis, and G. magniros‐tris)feedonsmall/soft,medium,andlarge/hardseeds,respectively,andaccordinglyhaveevolvedsmall,medium,andlargebeaks.Theclosely relatedcactus finch (Geospiza scandens) specializesonthenectar,pollen,andseedsofOpuntiacactiandhasevolvedanelon‐gatedbeak(SupportingInformationFigureS1).Resourcepartition‐ing has also promoted intra‐specific adaptive divergence withinthemediumground finch,where twobeak‐sizemorphsonSantaCruzIslandhavedivergedsignificantlyinecological(DeLeónetal.,2014,2012),morphological (Hendryetal.,2006;Hendry,Huber,León,Herrel,&Podos,2009;Huber,Leon,Hendry,Bermingham,& Podos, 2007), and genetic attributes (Chaves et al., 2016; DeLeón, Bermingham, Podos, &Hendry, 2010;Huber et al., 2007).Resourcepartitioninghas also been associatedwithmorphologi‐cal divergencebetweenhighlandand lowlandpopulationsof thesmallgroundfinchesonSantaCruzIsland(Kleindorfer,Chapman,

    urbanization. Overall, our findings accentuate the fragility of the initial stages ofadaptive radiation in Darwin’s finches and raise concerns about the fate of theGalápagosecosystemsinthefaceofincreasingurbanization.

    K E Y W O R D S

    adaptivedivergence,Galápagos,humandisturbances,maladaptation,nichepartitioning,resourcedistribution,urbanecology,urbanization

  •      |  3DE LEÓN Et aL.

    Winkler,&Sulloway,2006;Sulloway&Kleindorfer,2013).Studieson the continuum of intra‐ to inter‐specific divergence in thegroundfinchescanhelprevealtheprocessesunderlyingadaptivedivergenceandhowitmightbeinfluencedbyurbanization.

    Previousworkonthemediumgroundfinchsuggeststhatdiver‐genceof themorphshas recentlydiminishedat sitesadjacent toahumansettlement(Hendryetal.,2006).Ithasbeenhypothesizedthattheapparentrecentfusionofbeak‐sizedistributionsofthemorphs,from bimodal to unimodal,was due to the introduction and readyavailabilityofhumanfoods,whichmightbeflatteningtheadaptivelandscapeandtherebyreducingselectionagainstintermediateforms(DeLeónetal.,2011;Hendryetal.,2006).Acriticaltestofthishy‐pothesiswouldinvolveaskingwhethernichesegregationandfeedingpreferencesactuallydifferbetweenurbanandnon‐urbancontexts.

    Inthepresentpaper,weoffersuchatest,byconductingfeedingob‐servationsandfieldexperimentsoncoexistinggroundfinchspeciesatsitesthatspandifferentdegreesofurbanization.

    2  | METHODS

    2.1 | Field sites

    SamplingandexperimentstookplacebetweenJanuaryandMarchof 2014 and 2015 at four sites on Santa Cruz Island, Galápagos,Ecuador(Figure1).Allfoursitesarelocatedwithinthelow‐elevationaridzoneoftheisland(Wiggins&Porter,1971)anddifferedintheirdegreesofurbanizationaswellashuman‐associatedactivities(i.e.,thetendencyofpeopletofeedfinches;seeTable1fordetails).The

    F I G U R E 1  Finchesfeedingonhumanfoodsaturbansites.Panelsshowafemalemediumgroundfincheatingdryricefromafeeder(a).StudysitesonSantaCruzIsland,Galápagos,Ecuador,withurban(blackdots)sites,non‐urbansites(graydots),androads(lines)designedforvehiculartraffic(b).SantaRosaandBellavistawerenotincludedinourstudy,butareshownhereforillustrativepurposeonly.AgroupofsmallgroundfinchesfeedingcrumbsoffaplateatrestaurantinPuertoAyora(c).Photocredit:L.F.DeLeón

    (a)

    (c)

    (b)

    TA B L E 1  LevelofurbanizationandhumanbehaviorateachstudysiteonSantaCruzIsland,Galápagos,Ecuador

    Site Urbanization level Annual visitors Tendency of feeding Human contact

    ElGarrapatero Non‐urban Onlyscientistsvisitthissite

    Nohumanfeeding;lowhumandensity

    Minimalcontactwithhumans,exceptforscientistsandparkrangers

    ElGarrapateroBeach

    Non‐urbantourist 38,542 Regularhumanfeeding;lowhumandensity

    Humansvisitbeachforthedayandbringsnacks/picnicsastherearenoshops

    AcademyBay Intermediateurban 78,555 Littlehumanfeeding,butfinchesfeedopportunis‐ticallyonfoodscraps,andarelikelytobeintentionallyfedonoccasions;highhumandensity

    Humansvisitresearchcenterandareadvisednottofeedthefinches,butfinchesareoftenwithincloseproximitytolargegroupsofpeople

    PuertoAyora Urban 158,339 Regularhumanfeeding;highhumandensity

    Humansincitygeneratefoodscrapsonanhourlybasis

    Note.Sitesarerankedaccordingtothetendencyofhumanstofeedfinches(tendencyoffeeding)andthedegreeofinteraction(humancontact)withhumansateachsite.DatafortheannualnumberofvisitorswereobtainedfromDireccióndelParqueNacionalGalápagos&ObservatoriodeTurismodeGalápagos(2016).

  • 4  |     DE LEÓN Et aL.

    foragingecologyandfoodpreferencesoffinchesarelikelytodifferintransitionorhigh‐elevationsites,andtherefore,responsestour‐banizationmayalsodifferinthesezones.

    Thefirstsite,ElGarrapatero(EG;“non‐urban”site;0°41’16.6"S90°13’19.4"W), is located 1–2km inland of the island’s easterncoastandisabout10kmfromthenearestmajorhumansettlement(Bellavista,Figure1).Introducedplantspeciesandhumanfoodsarerareatthissite(DeLeónetal.,2011),althoughhumanactivityhasin‐creasedsince2009duetothepavingofaroadthatprovidesaccesstothecoast.Onatypicalday,dozensofvehiclesnowpassthroughthesite.Browsingbyferalgoatsanddonkeyswashistoricallycom‐mon at EG, but eradication efforts ledby theGalápagosNationalPark(Phillips,Wiedenfeld,&Snell,2012)haveresultedindecreasedgrazingdisturbance.Surveysatthissitewereperformedinanareaof~0.5km2eastwardfromEGroad.

    Thesecondsite,EGBeach(“non‐urbantourist”site;0°41’39.9"S90°13’15.8"W),hereafter referred toas “EGBeach,” is locatedontheeasternshoreofthe islandadjacenttothefirstsite (Figure1).Thenumber of visitors to this site has increasedmarkedly due tothenewlypaved road,whichprovidesdirect access to thebeach.Although this site supports nopermanent humanpresence, infra‐structure has expanded over the past 6years to include a gravelparking lot,cobblestonepaths,arangeroutpost,andanovernightcampingground.Typically,5–20touristsaday(althoughsometimesmanymore)visitthebeachtoswim,kayak,picnic,andobservewild‐life.Weincludedthissitetohelpdisentangletwourbanfactors:thelarge‐scalealterationofhabitats(absenthere)versustheoccasionaltoregularpresenceofhumansthemselves(presenthere).

    The third site, Academy Bay (AB; “intermediate urban” site;0°44’31.6"S90°18’15.3"W),issituatedonthesouthcoastoftheis‐landand is contiguouswith the townofPuerto Ayora (PA).Humaninfluences at AB include wide cobblestone and dirt paths, a highabundanceofexoticplantspecies,andthepresenceofhumanfoodsassociatedmainlywithconcessions for touristsvisiting theCharlesDarwinResearchStation(CDRS),aswellasafewlocalresidentsanddorms.Finchesatthissiteareregularlyobservedconsuminghumanfoods(Figure1)anddrinkingfreshwaterfromtortoisepensandbro‐kenpipes(DeLeónetal.,2011).Surveysatthissitewereperformedinanareaof~0.5km2encompassingtrailsfromthepublicentranceoftheGalápagosNationalParkeastwardtoacliffbehindtheanimalfacilitiesoftheCDRSanddidnotincludethebeachareasborderingtheCDRS.

    Thefourthsite,PA(“urban”site;0°44’34.8"S90°18’43.4"W),isthelargesthumansettlementonGalápagoswithover12,000inhab‐itants(InstitutoNacionaldeEstadísticayCensos).Puerto Ayoraalsoreceivesmanymoretouriststhanother islands intheArchipelago,with~218,365,and241,800recordedvisitorsin2016and2017,re‐spectively(DireccióndelParqueNacionalGalápagos&ObservatoriodeTurismodeGalápagos,2016,2017).At this site,wehave seenfinches feedingonawidevarietyof introducedplant speciesandhuman foods (Figure 1), including bread, potato chips, ice‐creamcones,rice,andbeans(DeLeónetal.,2011).Surveysatthissitewereperformedinanareaof~1.0km2encompassingthefirestation,the

    farmer’smarket,thecemetery,thepublicdock,andtheentrancetothetrailtoTortugaBay.

    Giventhecomplexwaysinwhichfinchescouldinteractwithhu‐mansonSantaCruz Island (Table1),wecannot considerour foursampling sites as representing a simple urbanization gradient.Weratherconsiderthemasfourdiscretesitesthatvaryindependentlyinboththedegreeofurbanization(asgivenbyhumaninfrastructureandpopulationdensity)andthepotentialforhumaninteractionwithfinches(afunctionofboththenumberandbehavioroftourists).

    Regarding human interaction with finches, reports from theGalapagos National Park indicate that the number of visitors totheGalápagosishighduringtheentireyear,withtwointer‐annualpeaks: the first between July and September, and the second inMarch (Dirección del Parque Nacional Galápagos & ObservatoriodeTurismodeGalápagos,2016,2017).Thus,oursamplingperiod(January–March)occurredjustbeforetheonsetofthesecondlarg‐estpeakinthenumberofvisitors.Althoughwedidnotquantifyfoodavailabilityinthecurrentstudy,finchesinurbanareasarelikelytoenjoyasurplusofhumanfoodsthroughouttheyear.However,wedonotexpectthatthissupplywasanyhigherduringoursamplingperiod.Furtherstudieswillbenecessary,however,tobetterunder‐standhowfinchpreferencesforhumanfoodsmightrespondtotem‐poralvariationintheavailabilityofbothnaturalandhumanfoods.

    2.2 | Feeding observations

    OurfirstgoalwastoquantifythedietsatourstudysitesofthefourGeospizaspecies(G. fortis,G. fuliginosa,G. scandens, and G. magniro‐stris).Towardthisend,weemployedapointobservationmethod(DeLeónetal.,2014,2011,2012).Briefly,duringmorningorafternoonhours,wewalkedalongpredeterminedtransectsandusedbinocu‐larstoidentifybirds(tothespecieslevel)and,ifpossible,thefooditemsonwhichtheywerefeeding.Atthreeofoursites,wesurveyedalongatotalof74transectscoveringalineardistanceof30.74km:EG(n=22,meanlength=436.80m),AB(n=22,476.75m),andPA(n=30,353.84m).NofeedingobservationsorestimationsofbirddensitywereperformedatEGBeachbecausethissiteisrepresentedby an open sandy beach with little natural vegetation. Transectcoursesweredeterminedrandomlyatthebeginningofeachwalk,buttheywerelimitedtoaseriesofpreexistingtrailsthatfacilitatedaccesstositeswithdensevegetation(EGandAB).InthetownofPA,transectsweredeterminedbyfollowingbothlargeandsmallstreetsthrough the middle and around the town, including surroundingneighborhoods(MirafloresandElEdén).Observationsinthisareain‐cludedfinchesfoundonthestreets,sidewalks,andrestaurantareas,aswellasonthenaturalvegetationofparks,gardens,androadsides.

    Food items includedspecificplantspeciesandplantparts (i.e.,seeds,fruits,leaves,orflowers)aswellasdifferenttypesofhumanfoods.We also recorded the category “ground,”when birdswerefeedingontheground,buttheexactfooditemscouldnotbeidenti‐fiedowingtotheirsmallsize.Afterafeedingeventwasrecorded,wemovedimmediatelyontothenextindividualtoavoidpseudoreplica‐tion.Ourdatathereforerepresentcountsofdiscreteobservations

  •      |  5DE LEÓN Et aL.

    ofindividualbirdsfeedingonparticularfooditems(DeLeónetal.,2014,2012 ).Finally,wegenerated rarefactioncurves tovisualizehowthecumulativenumbersoffooditemsobservedvariedinrela‐tiontooursamplingeffortsateachsite.

    2.3 | Bird density

    Oursecondgoalwastoestimatevariationinbirddensityacrosssites.Forthistask,weusedbirdcountdataforourfocalspeciesfromourfeedingobservationtransects,giventhatwerecordedallbirdswithin30m at each side of the observer, whether they were feeding ornot.Wethenusedthesevaluestoestimatethenumberofindividu‐alsperunitarea(Emlen,1977).Twofactorscouldhaveaffectedourestimatesofbirddensity.Thefirstisbirddetectabilityatsiteswithdensevegetation,suchasEGandAB,incontrasttothemoreopenurbansite(PA).Andsecond,combiningfeedingobservationsandbirdcountalongthesametransectmightnotbeasaccurateassurveysdedicatedtobirdcountsalone.However,ourmaingoalherewastoestimate relativedifferences inbirdabundancebetweenurbanandnon‐urbanenvironments,ratherthanprovidingaprecisevalueofbirddensityateachsite.Inaddition,toreduceautocorrelationeffectsandtoimprovedetectabilitywerecordedonlyonefeedingeventperindi‐vidual(seeabove),andonlywithin30moftheobserver.ThesetypesofobservationswerealsofacilitatedbythefactthatDarwin’sfinchesaretameandcanbeeasilyobservedatshortdistanceswithlittlein‐terference(DeLeónetal.,2014;Grant,1999).

    2.4 | Finch response to food cues

    Totestwhetherandhowfinchesacrossourstudysitesrespondtothepresenceofpeople,wedevelopeda “finch–human interaction”experiment.We recorded finch responses to two different humanstimuli:avisualstimulus(anexperimenterstandingorsittingstillandquietlyinanopenspace)andanaudiovisualstimulus(anexperimenterstandingorsittingstillandnoisilyrustlingabagofpotatochips,gen‐eratinga“crinkle”soundtypicallyassociatedwithpackagedhumanfoods). Includingthissecondstimuluswas inspiredbyobservationsof finches approaching humans opening and/or handling packagedfoods.Thestimuliwerepresentedsequentiallyandinthesamespot,withthevisualstimulusfirst(5min)andtheaudiovisualstimulussec‐ond(fivemoreminutes).Duringstimuluspresentation,werecordedthenumber,species,andsexofallbirdsthatapproachedwithin1.5moftheexperimenter,includingbirdsthatperchedabovetheexperi‐menter.Presentation locationswithinour siteswere selectedhap‐hazardlyandwereconductedatleast100mapartfromeachotherduringagivenday.Dataforthisexperimentwerecollectedatallfoursites:EG(non‐urban,n=22),EGbeach(non‐urbantourist,n=37),AB(intermediateurban,n=14),andPA(urban,n=30).

    2.5 | Feeding preference experiment

    Toquantify finch feedingpreferences,andwhetherandhowtheyvaried with the degree of urbanization, we performed replicate

    “cafeteria” experiments, in which finches were presented with achoiceofhumanandnativefooditems.Weconstructedcardboardfeedingtrays(30cm×30cm)withninesections(3×3gridpattern)intowhich food couldbeplaced.A rockwasplaced in the centersectionofeachtrayasananchor.Eachtraywasstockedwith2.5gof each of six natural or human foods commonly observed previ‐ously(DeLeónetal.,2014,2011,2012).Tocontrolforanypotentialbiasesassociatedwiththelocationoffoodonthetray,fooditemswereplaced randomly in six of the eight available sectionsof thetray.Humanfooditemsincludeduncookedwhiterice,potatochips,andcoconutcookies,thelattertwoofwhichwecrumbledintosmallpiecestomimicthesizeandshapecommonlyseeninurbansites.Fornaturalnativefoods,weincludedfruitsfromCryptocarpus pyriformis,Tournefortia psilostachya, and Scutia spicata.Wechoosethesethreeplantspeciesbecausetheyoccurcommonlyateachofoursitesandareeatenfrequentlybyallgroundfinches,regardlessoftheirbeaksize(DeLeónetal.,2014).Furthermore,theyallproducesmallandsoftseeds,andthereforearecomparabletohumanfoodsintermshardness,andareunlikelytoimposefunctionalconstraintsonfinchfeeding.Wedidnotincludeadditionalsoftfooditemssuchasinsectlarvaeinourexperimentsbecausetheirmostimportantcontributiontofinchdietislimitedtotheonsetoftherainyseason(DeLeónetal.,2014);thus,theyrepresentalessstablefoodresourceforfincheswhencomparedwithothernaturalandhumanfoodsitems.Thetraywasplacedontheground,andobserversmovedatleast10mawayorconcealedthemselvesatleast5mawaytorecordfeedingactivity.Wedidnotpresentemptytraysinourtrialsbecausewewereinter‐ested in finchpreference for different types of foods rather thanfinches’reactionstothepresenceoffoodingeneral.Trialsiteswereselectedhaphazardly,andnotrialswereconductedwithin100mofeachotherduringthesameday.Trayswereleftoutforamaximumof20minifnofinchapproached.Ifafinchapproachedandfedfromthetray,atimerwasstartedandobservationsrecordedfor10minfromthefirstfinchfeeding.Werecordedthetotalnumberoffinchesthatapproached,perchedon,and/orfedatthetray,andtheirspe‐ciesidentity.Attheendofeachtrial,trayswerecollectedandthefoodthatremainedineachsectionre‐weighed.Weperformedtrialsatallfoursites:EG(n=34),EGbeach(n=40),AB(n=31),andPA(n=46).Overall,ourexperimentswerenotdesignedtodisentanglethemechanismsunderlyingnaturalfeedingpreferencesinDarwin’sfinches,butrathertotestwhetherornotDarwinfinchesshowpref‐erencesforhumanfoodsovernaturalfoodsinbothurbanenviron‐mentsandnon‐urbanenvironments.

    2.6 | Data analysis

    Tocharacterizevariation in finchdietsacrosssites,weperformedcorrespondenceanalysis(CA)onourfeedingobservationdata.CAisamultivariatedescriptiveanalysisbasedonmatricesoffrequencydata(Benzécri,1973).WehereusedCAtovisualizeanddeterminethecontributionofeachfooditemtothetotaldietofeachspeciesateachsite.Wethenusedcosine‐squared(Cos2)correlations(Rpack‐ageFactorMineR;Lê,Josse,&Husson,2008)totestforassociations

  • 6  |     DE LEÓN Et aL.

    amongfooditemsandfinchdiets.Totestforvariationinbirddensityacross sites,weperformedaKruskal–WallisH test, followedbyaposthocDunntestformultiplecomparisons.

    To assess among‐site variation in finch response to humans,we ran two tests. First,we tallied the number of birds approach‐ing human experimenters in the response trials and performed aKruskal–Wallistestonthesetallies.Second,foreachsitewecalcu‐latedtheproportionoftrialsinwhichatleastonefinchapproachedthestimulus,relativetothetotalnumberoftrialsperformed(pro‐portion positive response) and performed a chi‐squared test ontheseproportions.

    Toanalyze feedingpreferences fromourcafeteriaexperiment,we constructed a nested linearmodel to test for variation in theamountoffoodeaten(ingrams)acrosssites,foodcategory(humanvs.natural),fooditemnestedwithinfoodcategory(ricevs.chipsvs.cookiesforhumanfoodsandC. pyriformisvs.T. psilostachyavs.S. spi‐catafornaturalfoods),andthetwo‐wayinteractions(site×foodcat‐egory and site×food item).Thenumberofbirds that approachedtraysinthecafeteriaexperimentsprovideduswithathirdmetricofresponse,beyondthetwonotedinthepreviousparagraph.

    Totestforsite‐specificvariationindietarynichepartitioning,weestimatedateachsitetwocommonlyconsiderednicheparam‐eters:nichewidthwithineachspecies,andnicheoverlapbetweeneach species pair. Analyses were performed across all groundfinchestogether(n=1,063)andforthetwogroundfinchspeciesthathad thehighest sample sizes (G. fortis [n=571]andG. fulig‐inosa [n=349]) (Table2).Toestimatenichewidth,wecalculatedShannon’s (Colwell & Futuyma, 1971) and Levin’s (Levins, 1968)nichewidthindicesasimplementedintheRpackagespaav.0.2.2

    (Zhang,2016).Toestimatenicheoverlap,wecalculatedPianka’s(1973) niche overlap indices as implemented in the R packageEcoSimR (Gotelli&Ellison,2013).These indices rangefromzerotoone,withzero indicatingnooverlap infooditemsacrossspe‐ciesandoneindicatingcompleteoverlap.FollowingDeLeónetal.(2014),wenextusedEcoSimRtogeneratenullmodelsofexpectedniche overlap under different randomization algorithms (Gotelli&Entsminger,2009).Withthesemodels,wetestedwhetherob‐servednicheoverlapbetweenspeciesdifferedsignificantlyfromrandom expectations.We generated 1,000 permutations underthe RA3 algorithm (Lawlor, 1980). The RA3 algorithm is recom‐mended fornicheoverlapestimatesbecause it randomizeseachspecies’ prey items, while maintaining its overall niche breadth,thus generating a random utilization matrix with similar dimen‐sionsastheobservedmatrix(Gotelli&Entsminger,2009;Lawlor,1980).AlldataanalysisandgraphingwereperformedinRversion3.3.0 (RCoreTeam,2013).Researchpermits for thisworkwereobtained from theMinistry of Environment of Ecuador and theGalápagos National Park (Permits No. PC‐29‐14 and PC‐25‐15).Thisstudywasalsoconductedfollowingtheguidelinesofthean‐imalcareprotocoloftheUniversityofMassachusetts,Amherst.

    3  | RESULTS

    3.1 | Feeding observations and bird density

    Duringthe2yearsofourstudy,wecollectedatotalof1,213feed‐ing observations: 166 at EG, 491 at AB, and 556 at PA (Table 1;SupportingInformationTableS1).Thetotalnumberofdifferentfood

    TA B L E 2  Numberoffeedingobservationsacrossthreesitesand11passerinebirdspeciesonSantaCruzIsland,Galápagos,Ecuador

    Species Common name

    El Garrapatero Academy Bay Puerto Ayora

    TotalHuman Natural Human Natural Human Natural

    Geospiza fortis Mediumgroundfinch

    3 102 9 173 227 57 571

    Geospiza fuliginosa Smallgroundfinch 31 11 133 152 22 349

    Geospiza magnirostris Largegroundfinch 3 3 5 11

    Geospiza scandens Cactusfinch 6 4 30 7 8 55

    Geospiza spp. Groundfinch 16 6 24 30 1 77

    Geospiza parvula Smalltreefinch 2 7 10 1 20

    Platyspiza crassirostris Vegetarianfinch 5 3 72 11 15 106

    Crotophaga ani Smooth‐billedani 1 1 2

    Setophaga petechia Yellow warbler 1 8 3 12

    Mimus parvulus Galápagosmockingbird

    1 5 6

    Myiarchus magnirostris Galápagosflycatcher

    2 2 4

    Total 3 163 34 457 441 115 1,213

    Note.Observationsofotherspeciesareincludedhereforreference,butonlydatafromgroundfinches(Geospiza spp.)wereincludedinourstatisticalanalyses.Whenidentificationtospecieslevelwasnotpossible,weincludedaGeospiza spp.category.Foreachobservation,wereportedeachfooditem’sorigin,naturalversushuman.

  •      |  7DE LEÓN Et aL.

    itemsweobservedfincheseatingcorrespondedroughlytodegreesofurbanization,from13atEGto31atABto36atPA(Table1andSupporting Information Table S1). The greater diversity of foodtypesatthelattersitesisduemostlytothepresenceatthesesitesofavariety(11items)ofhumanfoods(Table1;SupportingInformationTableS1).Bycontrast,thediversityofnativeplantspeciesconsumedwassimilaracrosssites,consistentwithfindingsfromourprevious5‐year survey at EG andAB (De León et al., 2014). Although thenumber of feeding observations varied across sites, rarefactioncurves showedevidence for saturationat a relatively lownumberofobservations(~150)foreachsite(SupportingInformationFigureS2),suggestingthatoursamplingeffortwassufficient toestimatedietarynichesingroundfinches.Thiswasalsoconsistentwithapre‐vious5‐yearstudyoffeedingpreferenceattwoofthesamesites(EGandAB)(DeLeónetal.,2014).

    For our transect surveys, we observed a total of 3,343 indi‐viduals (both feeding and non‐feeding) during 75.1hr (SupportingInformation Table S2). The density of ground finches varied sig‐nificantly across sites, mean±SE: 761.37±81.55bird/km2 at EG,923.69±75.33bird/km2 at AB and 1,019.17±104.65bird/km2 atPA;Kruskal–Wallis test:χ2(2)=8.23,p=0.016,withposthoctestsconfirming a significant difference between the most‐urbanizedsites(PA)andboththeleast‐urbanizedsite(EG,p=0.003)andtheintermediate‐urbanizedsite(AB,p=0.027).

    Correspondenceanalysesprovidedafurtherillustrationofhowfinches consumed human food itemswith increasing urbanization(Figure2,notehowspeciesat theurbansite,PA,clusternear thehumanfood items,shownasredfilledcircles).Somehumanfoods

    contributeddisproportionatelytothefinchdietaturbansites,butalmostneveratnon‐urbansites (Figure2;Supporting InformationTable S1). At PA in particular, finches were observed feeding al‐most exclusively (78.6% of all observations) on human foods, in‐cluding crackers (3.7%), rice (5.7%), bread (6.6%), andunidentifiedcrumbs(46%),aswellasintroducedgardenspeciessuchasHibiscus sp. (1.6%), and Delonix regia (Flamboyant; 10.5%). At AB, finchesoftenfedonnativeplantspeciessuchasBoerhavia caribaea,S. spi‐cata,Cryptocarpus pyriformis, and Cordia lutea, but they alsowereseenfeedingonsomehumanfooditemssuchasbreadandcrumbs(Supporting Information Table S1). Finches at this site were alsoseendrinkingfreshwaterfrombrokenpipes.Incontrast,atthenon‐urbansite(EG)fincheswereseenfeedingalmostexclusivelyonna‐tivespeciessuchasS. spicata,C. pyriformis,Cordia leucophlyctis,andT. psilostachya(Figure2,SupportingInformationTableS1).TheonlyexceptionswerethreebirdsonthesideoftheroadtotheEG,whichwereseenpeckingatacandywrapperandcrumbsleftbytourists(Figure2,SupportingInformationTableS1).

    3.2 | Finch response to food cues

    Our finch–human interaction trials revealed significant varia‐tion across sites in finches’ response to thepresenceofpeople,Figure3;Kruskal–Wallistest:χ2(3)=60.68,p<0.001.FewfinchesapproachedtheexperimentersatEG(non‐urbansite)andAB(in‐termediate‐urbansite),yetmanyfinchesapproachedtheexperi‐menteratPA(urbansite),suggestingthaturbanbirdsareindeedmoreaccustomedtothepresenceofhumans.Interestingly,aneven

    F I G U R E 2  DietofgroundfinchesacrosssiteswithdifferentdegreesofurbanizationonSantaCruzIsland,Galápagos,Ecuador.Thegraphrepresentscorrespondenceanalysis(CA)basedonfeedingobservationdata.Colorsrepresentnatural(green)andhuman(red)fooditems.Blacklabelsrepresentspeciesandsitecentroidcombinations:ElGarrapatero(EG),AcademyBay(AB),PuertoAyora(PA),Geospiza fortis (FOR),Geospiza fuliginosa(FUL),Geospiza magnirostris(MAG),andGeospiza scandens(SCA).Fooditemslabelsandpointswereslightlyoffsettofacilitatereadability.Inthisgraph,thepositionofeachspecies/sitecombination(filledtriangles)correspondstothefooditemsfavoredinitsdiet.Finchesattheurbansite,PA,clusternearthehumanfooditems

    ABFOR

    ABFUL

    ABMAG

    ABSCA

    EGFOR

    EGFUL

    EGSCA

    PAFOR

    PAFUL

    PAMAG

    PASCA

    −2

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    0 1Dim1 (29%)

    Dim

    2 (2

    0.6%

    )

  • 8  |     DE LEÓN Et aL.

    stronger response (approach to an experimenter) was observedat the non‐urban tourist site, EG Beach (Figure 3; SupportingInformationTableS3).Withineachsite,wedidnotfindstatisticaldifferences infinchresponsebetweentheaudiovisual thevisualstimulusalone (Figure3;p>0.05 forall comparisons).However,becausetheorder inwhichwepresentedthestimuli (visualfirstandthenaudiovisual)wasfixedratherthanrandomized,wewereunable to distinguish the contribution of either of the stimulusfromeffect of longer exposure to the first stimulus to finch re‐sponse.Nevertheless,theoveralldifferencesamongsitesinfinchresponse to the presence of humans were corroborated by theproportion of positive responses (the number of trials in whichat leastonefinchapproachedthestimulus),whichvariedsignifi‐cantlyacrosssites,χ2(3)=56.27,p<0.001,withupto73%,35%,and20%atEGBeach,PA,andAB,respectively,andonly7%atEG.

    3.3 | Feeding preference experiment

    Thecafeteriaexperimentdatarevealedastrikingvariationinfeed‐ingpreferencesacrosssiteswithdifferentdegreesofurbanization(Figure 4; Supporting InformationMovies S1 andMovie S2). Theamountoffoodconsumedfromourexperimentaltraysvariedsub‐stantiallyacrosssites,foodcategories,andfooditems,with“site”interacting significantlywithboth foodvariables (Table3).AtEG(non‐urban site), only one individual inspected our feeding trays(Figure 3), but no food consumptionwas observed across any ofthetrials(Figure4),evenwhenfincheswereinthevicinity.AtEGBeach (non‐urban, tourist site), finches preferentially consumedhuman foods over natural foods (Tukey’sHSD:p<0.001). At AB(intermediate urban site), finches showed intermediate responsestoourfeedingtrays(Figure4;Tukey’sHSD:p=0.948),withanap‐parentstrongpreferenceforriceoverallothernativeandhumanfooditems(Figure4).AtPA(urbansite),finchesshowedthestrong‐estpreference forhumanfoodsovernative food items (Figure4;Tukey’sHSD:p<0.001).Wefoundthatthenumberoffinchesap‐proachingtheexperimentaltrayswasloweratEGandABthanatPAandEGBeach(Figure3).Thisvariationwassignificantacrosssites,χ2(3)=57.14,p<0.001,andshowedstrongdifferencesbetweenEG(non‐urban)andPA(urbansite)aswellasbetweenEGandEGBeach(non‐urbanbuttouristsite)(SupportingInformationTableS3).

    3.4 | Dietary niche partitioning

    Across sites, variations in resourceuse led tohighly variable esti‐matesofnichebreadthwithin speciesandnicheoverlapbetweenspecies.InthecaseofG. fortis and G. fuliginosa,nichebreadthswerelowestatEG(non‐urbansite),intermediateatAB(intermediateurbansite),andhighestatPA(urbansite;Figure5),consistentwithvaria‐tioninfoodtypediversity.Withrespecttodietpartitioningbetweenthesetwospecies,finchesatEG(non‐urbansite)andAB(interme‐diate urban site) showed lower diet overlap than expected fromrandomsimulations(Figure5),whereasthetwofinchspeciesatPA(urbansite)showednearly100%dietoverlap,greaterthanexpectedatrandom(Figure5).Similartrendsemergedinanalysesofallgroundfinchspecies,bothfornichebreadth(SupportingInformationFigureS3)andfornicheoverlap(SupportingInformationFigureS4).

    4  | DISCUSSION

    Our main results were as follows: (a) finch density was notablyhigheraturbansitesthanatnon‐urbansites;(b)foodtypeavailabil‐ityandthedietoffinchesaturbansiteswerenotablybroaderthanatothersitesandincludedmanyhumanfoods;(c)finchesatsitesfrequentedby people (the urban sites and the non‐urban touristsite)werewillingtoapproachpeopleandnovelobjects(foodtrays),muchmoresothanwerefinchesatthenon‐urbansite;(d)thede‐greeofurbanizationandthepresenceofhumansassociatecloselywith strong preferences for human foods, with finches at urban

    F I G U R E 3  FinchresponsetohumansacrosssiteswithdifferentdegreesofanurbanizationandhumanbehavioronSantaCruzIsland,Galápagos,Ecuador.Thedatarepresentthenumberoffinches(mean±SD)thatapproachedthehumanexperimenter(toppanel,foodpreferencetests)andthefoodtray(bottompanel,cafeteriaexperiment)atthefourstudysites.SitelabelsareElGarrapatero(EG),ElGarrapateroBeach(EGBeach),AcademyBay(AB),andPuertoAyora(PA)

    0

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    EG EG Beach AB PA

    VisualVisual + auditory

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  •      |  9DE LEÓN Et aL.

    sitesfeedingpredominantlyonhumanfoods.Fromthesefindings,wecansurmisethatfinchpreferencesforhumanfoodsinurbanen‐vironments,andcorrespondingalterationstotheirbehavior,haveatleastforthemomentcollapsednichedifferencesthatnormallycharacterize the adaptive radiation of Darwin’s ground finches.Theseresultsalsosuggestthaturbanizationandthe introductionof novel ecological resources aremodifying finch adaptive land‐scapesandbehavior,inwaysandtodegreesthatseemlikelytoun‐derminethenaturalprocessesthatdriveadaptivediversification.

    4.1 | Behavioral flexibility and adaptation to urban environments

    Urbanization often alters the distribution of ecological resources(McKinney, 2002, 2006 ; Schochat, Warren, Faeth, McIntyre, &

    Hope, 2006) and represents a novel and strong agent of selec‐tion towhich organismsmight ormight not adapt (Alberti, 2015;Atwell et al., 2012; Smith&Bernatchez, 2008).Oneway that or‐ganisms could cope with altered resources is through behavioralflexibility,definedastheabilityoforganismstoaltertheirbehaviorinresponsetochangingenvironments(Coppens,Boer,&Koolhaas,2010).Behavioralflexibilityisexpectedtofacilitatetheexplorationof novel ecological resources (Inouye, 1978; Sol et al., 2014; Sol,Lefebvre,&Rodríguez‐Teijeiro,2005;Sol,Timmermans,&Lefebvre,2002; Tebbich, Sterelny,& Teschke, 2010;Wright et al., 2010), inbothnaturalenvironments(Liebl&Martin,2014;Nicolakakisetal.,2003;Soletal.,2005)andurbanenvironments(Bowers&Breland,1996;Gotanda, Sharpe,& Léon, 2015; Lowry et al., 2013;Martin&Fitzgerald,2005;Schochatetal.,2006;Soletal.,2014).Inbirds,behavioralflexibilityinurbanenvironmentsissometimesassociatedwithareductioninneophobia(Atwelletal.,2012;Boogert,Reader,&Laland,2006;Martin&Fitzgerald,2005;Soletal.,2014)andtheincorporationofnovelhumanfoodsintodiets(Boogertetal.,2010;Ducatezetal.,2015;Shochat,Lerman,Katti,&Lewis,2004;Soletal.,2002;Sol,Griffin,Bartomeus,&Boyce,2011;Sol, Lapiedra,&González‐Lagos,2013).

    Consistent with these findings from other systems, we foundthatDarwin’sgroundfinchesinurbanenvironmentsareaccustomedtothepresenceofpeopleandalsodisplayastrongpreferenceforhumanfoods,incontrasttofinchesfromnon‐urbanenvironments.Inaddition,thefactthatfinchesaturbansiteslargelyignorednaturalfoodsfromexperimentaltrayssuggeststhatbehavioralflexibilityisfacilitatingspecializationonhigh‐calorieandeasilyaccessiblehumanfoods.Forinstance,thestrongpreferenceforriceatAB(Figure4)couldreflectacanalized/learnedbehavior,giventhatfincheshavepreviously—on many occasions—eaten rice at this site, furnished

    F I G U R E 4  Finchespreferhumanfoodatsiteswheretheyarefedbyhumans.ThegraphshowstheMean±SEoffoodeatenfromexperimentalcafeteriatraysatfourdifferentsiteswithdifferentdegreesofanurbanizationandhumanbehavioronSantaCruzIslandintheGalápagos.Whiteindicateshumanfoods,andgrayindicatesnaturalfoods

    TA B L E 3  Finchfeedingpreferencesforhumanversusnaturalfoodsacrosssites

    Factors SS df F p

    Site 2.09 3 40.723

  • 10  |     DE LEÓN Et aL.

    bysourcessuchasbirdfeeders,directfeedingbypeople,andlocalrestaurants(DeLeónetal.,2011).Thecurrentfinchpreferenceforhuman foods could also reflect the influences of both behavioralflexibilityandexperienceoperatingatdifferentpointsoftime.Forexample,behavioralflexibilitymayhavebeenmostimportantasthefirstgenerationofurban“pioneers”expandedtheirdietstoincludehumanfoods.However,insubsequentgenerations,urbannestlingsraisedonhumandietsmayhavedevelopedapreferenceforthesefoodssimplybasedonexperience/familiarity.Nevertheless,wecan‐notdisentangle the relative importanceof these twomechanismswiththecurrentdata.Overall,however,thesefindingssupportthelikely importance of behavioral flexibility in promoting Darwin’sfinchadaptiveradiation(Grant&Grant,2008;Tebbichetal.,2010).

    Exploiting urban environments might present additional chal‐lengesfororganisms(Chamberlainetal.,2009;Lowryetal.,2013;McKinney,2006;McLaughlin,Janousek,McCarty,&Wolfenbarger,2014; Slabbekoorn & Peet, 2003), including negative effects on

    health that might reduce lifespan and probabilities of survival(Salmo,Nilsson,Nord,Bensch,&Isaksson,2016). Inaddition,con‐suminghighlyprocessedhuman foodssuchasbreadandcrackerscouldhavenegative impactson finchhealthorphysiological con‐dition (Jones, 2011;Murray et al., 2018), a possibility that shouldbe explored in further studies. Indeed, urban environments couldconstituteeffectiveecologicaltrapswhereorganismsexploitenvi‐ronmentswithnegativefitnessconsequences(Dwernychuk&Boag,1972).Inshort,whileourresultsclearlyshowashifttohumanfoodsinurbansites,theadaptivesignificanceofthatshiftremainstobedetermined.Examiningthephysiologicalandhealtheffectsofcon‐suminghumanfoodsseemscrucial tounderstanding thepotentialfitnessandevolutionaryconsequencesofurbanizationonDarwin’sfinches.

    4.2 | The urban finch and the future of adaptive radiation

    Accumulatingevidenceillustratesthatsomespeciesareabletoex‐ploitnovelresourcesprovidedbyurbanenvironments (Donihue&Lambert, 2014; Johnson&Munshi‐South, 2017; Kettlewell, 1955;Littleford‐Colquhounet al., 2017;Sol et al., 2002;Winchell et al.,2016). Less clear, however, are the evolutionary consequences ofusingthesenovelresourcesforpopulationsorspeciesundergoingadaptiveradiation.InDarwin’sfinches,theinteractionbetweenre‐source availability and competition for resources is thought to beessential for promotingdiversification and thenmaintaining coex‐istenceamongclosely relatedspecies (Bowman,1961;DeLeónetal., 2014;Grant, 1999; Lack, 1947; Schluter, 2000). Indeed, theseprocesseshaveledtotheformationofanumberofspecieswhosebeakmorphologyisdifferentiallyadaptedtofeedondifferentfoodresources(Bowman,1961;Grant,1999;Lack,1947;Schluter,2000).However,Darwin’s finchesmightalsobeconsideredopportunisticor“imperfectgeneralists”(sensuDeLeónetal.,2014)because,dur‐ingbenignperiods, theirdiets tend toconvergeon foods thatareabundantandeasilyaccessible,regardlessoftheirbeakmorphology,resultingintemporaryweakeningofselection(Abbottetal.,1977;Smith,Grant,Grant,Abbott,&Abbott,1978).Nevertheless,strongselectiononbeakmorphologyre‐emergesduringperiodsofdroughtorscarcity,whenfinchesspecializeonthefoodtypesforwhichtheyarebestadapted.Asaconsequence,year‐roundavailabilityofsoftandhighlyabundanthumanfoodsinurbanenvironmentsislikelytoaffecttheveryecologicalandevolutionaryprocessesthatpromotespeciesandphenotypicdiversificationinDarwin’sfinches(DeLeónetal.,2011;Hendryetal.,2006).

    As suggestedbyour results, in thepresenceof an abundanceofcalorie‐richandreadilyavailablehumanfoods,naturalinter‐spe‐ciesecologicaldifferencesmightbeeroding, leadingtosmoothingof the previously rugged adaptive landscape and a correspondingweakening of selection underlying divergence. This process hasbeeninferredpreviouslyadjacenttourbanenvironmentsonSantaCruz Island,wheredivergentmorphsof themediumground finchhave been progressively converging as the human population has

    F I G U R E 5  Nichecharacteristicsofgroundfinches(Geospiza fortis and Geospiza fuliginosa)acrosssiteswithdifferentdegreesofurbanization.ThedatarepresenttheShannon–Wiener'snichebreadth(toppanel)andPianka'snicheoverlap(bottompanel)indexestimatedfromfeedingobservationsatthreesitesonSantaCruzIsland,Galápagos,Ecuador.SitelabelsareElGarrapatero(EG),AcademyBay(AB),andPuertoAyora(PA)

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  •      |  11DE LEÓN Et aL.

    increased (DeLeónetal.,2011;Hendryetal.,2006).Ourpresentstudyshowshowtheeffectsofurbanizationandhumanbehaviormightalsoextendtoothergroundfinchspecies.Specifically,besideserodingecologicaldifferencesbetweenthesmall(G. fuliginosa) and medium(G. fortis)groundfinch,weobservedasubstantialnumberofcactusfinch (G. scandens,11 individuals)and largegroundfinch(G. magnirostris,55individuals)feedingonandrespondingtohumanfoodsat theurbansite.Furthermore,our finding that finchesatanon‐urbanbuttouristsite(EGBeach;SupportingInformationMovieS1)alsoelicitedastrongpreferenceforhumanfoodssuggeststhatecologicalnichesmightbemoresusceptibletohumandisturbancesthan previously thought. As such, changes in beak morphologywithinandacross species inurbanenvironmentscouldbe shapedbyreducedsurvivaldisadvantagesof intermediatebeak‐sizebirds,includinghybridindividuals,whichundernaturalcircumstancesareunlikely tosurvive (i.e.,becausethey fall invalleysof lowfitness).Oneremainingquestion iswhattheconsequencesofurbanizationandthepresenceofhumansatthelocalscalemightbefortheadap‐tiveradiationofDarwin’sfinchesasawhole?

    One likely short‐term consequence of urbanized adaptivelandscapeswill be the convergence of previously distinct speciesthrough introgressive hybridization (Rhymer & Simberloff, 1996;Seehausen,Takimoto,Roy,& Jokela, 2008;Taylor et al., 2006). Inthegroundfinches,hybridizationiscommonandhasbeendetectedin non‐urban habitats (Chaves et al., 2016; Grant, 1993; Grant &Grant,1989,1996;Lamichhaneyetal.,2015),suggestingalackofintrinsic genetic incompatibilities among species. During extremeclimaticconditions(i.e.,highrainfall)onDaphneMajor,whennaturalfoodsabound,hybridizationhasledtoconvergenceofspeciessuchas the cactus finchand themediumground finch (Grant&Grant,2002;Grant,Grant,Markert,Keller,&Petren,2004), andalso forthesmallandthemediumgroundfinch(Grant&Grant,2016).Intreefinches (Camarhynchus spp.), hybridization has also beendetectedon Floreana Island, likely associated with the introduction of thePhilornisparasite(Kleindorferetal.,2014;Peters,Myers,Dudaniec,O’Connor,&Kleindorfer,2017).Overall,thesestudiessuggestthatintrogressivehybridizationinDarwin’sfinchesiswidespread.Ifitisalso strongandpersistent, it could lead to thecollapseof speciesboundariesinhuman‐alteredenvironments.Anotherpotentialcon‐sequenceofhybridizationinurbanenvironmentsisthegenerationofnovelgeneticvariationthatcouldfacilitatefurtherdiversificationinDarwin’sfiches.Thiscouldoccur,forinstance,ifnovelhybridin‐dividualswith intermediatebeak sizesareable toexperiencehighfitnessbyspecializingonfooditemsofintermediatesize/hardness,such ashuman foods. It is important tomention that despite evi‐denceofhybridization,otheraxesofdivergencesuchasdifferencesinsongtypesandvocalperformance(Grant,1999;Huber&Podos,2006;Podos,2001)couldalsohelpmaintainspeciesboundariesinthe faceof increasingecologicaldisturbance.However,both songtypesandvocalperformancearetightlyassociatedwithbeakmor‐phology (Podos, 2001), suggesting that changes in selectionpres‐sureonbeaksviaalterationoffoodresourcescouldalsoaffectotheraxesofdivergence.

    Alterationofecologicalresourcesatlocalscalessuchasasin‐gleurbansiteonSantaCruzIslandcouldpotentiallyhavebroaderimplicationsforthegroundfinchradiationacrosstheentireisland.For instance, increasing finch population at the urban site couldpromotemergingofspeciesviageneflowandinterspecifichybrid‐ization (as above). This possibility was hinted at by our previousstudythatshowedthatgeneticdifferencesamonggroundfinches(G. fortis,G. fuliginosa, and G. magnirostris)aresmalleratAB(thein‐termediate‐urbansite)thanatEG(thenon‐urbansite)(DeLeónetal.,2010),possiblydue tohighergene flowamongspeciesat theintermediate‐urbansite.Interestingly,G. fortis and G. fuliginosa are boththemostabundantandthemostcloselyrelatedspeciesacrosssites(Chavesetal.,2016;DeLeónetal.,2010),whichislikelytoam‐plifythemergingeffectofhybridizationinurbanenvironments.Inaddition,urbanfinchpopulationscouldbeasourceofmaladaptivegeneflow(Hendry,Taylor,&McPhail,2002),leadingtochangesintheoptimalbeak‐sizedistributionofnon‐urbanfinchpopulations.Werefer tomaladaptivetraitsas thosethat reducefitnessunderagivenenvironmentalcondition.Forinstance,urbanfinchescouldultimatelyevolvean“urbanbeakmorphology”(e.g.,asmallandsoftbill) adapted to exploit soft human foods in urban environments.Butindividualswiththatmorphologywouldfacealowerfitnessiftheymigratedtonaturalenvironmentswhereseedsarelargerandharder than human foods. In this context, hybridization (or geneflow)fromurbanenvironmentscouldrendernon‐urbanfinchpop‐ulationsunabletocopewithdrasticenvironmentalchangesundernaturalconditionsandcouldreinforcegeneticdifferencesbetweenurbanandnon‐urbanpopulations.Thus,wepostulatethatmaladap‐tationcouldbeanotherunintendedconsequenceofurbanization.

    4.3 | Possible evolutionary consequences of human behavior

    Studies of urbanization often highlight human population density,thepresenceof impervious surfacesor thedevelopmentof infra‐structure asmain drivers of effects on local biodiversity (Alberti,2015;Gaston,2010;Gotandaetal.,2017;Johnson&Munshi‐South,2017;McKinney,2006).However,humanbehaviorandthewayweinteractwith local biodiversity could expand impacts of urbaniza‐tionbeyondcitycenters.Thiswassuggestedbyourfindingofstrongfinch preferences for human foods at EGBeach, a non‐urban buttouristsitelocated~12kmawayfromthetownofPA.Thisalsosug‐geststhathumanbehaviorratherthanhumanpopulationdensityisthemaindriveroffinchpreferenceforhumanfoods.Althoughad‐ditional replication isneededtostatisticallydisentanglethesefac‐tors,wearguetheeffectofhumanbehavioronfinchdietsislikelyfacilitatedbyourtendencytofeedbirdseitherdirectly(viafeeders)or inadvertently (via fooddroppingor littering),bothofwhichareoftenseenatbothurbancentersandnon‐urbantouristsites(LF.DeLeón,per.obs).Inaddition,althoughtheGalápagosareaprotectedarea, and human infrastructure is rather localized, popular touristsitesoutsidetheurbanareasappeartoalsobeaffectedbythewayhumaninteractwithfinchesatthosesites.

  • 12  |     DE LEÓN Et aL.

    Theecologicalandconservation implicationsofwildlifefeedingandfoodprovisioninghavebeenexploredextensivelyacrossadiver‐sityoftaxa(Cox&Gaston,2018;Dubois&Cheptou,2017;Murrayetal.,2018).However,lessisknownabouttheevolutionaryimplicationsof such common human behaviors. Here, we showed thatwildlifefeedingandfoodprovisioning inDarwin’sfinchescould impacttheveryevolutionaryprocessthedrivediversificationinthisiconicbirds.

    Inconclusion,ourstudyfocusedonsingleurbancenteronasin‐gleisland,andthelackofreplicationlimitsourabilitytodrawgeneralinferences.Yet,ourstudyrepresentsafirstattempttoexplorethepotentialimpactsofurbanizationandhumanbehaviorontheongo‐ingadaptiveradiationofDarwin’sfinches.Wealsohypothesizethatasimilarphenomenonmightcurrentlybeaffectingfinchesinurbanenvironments across theGalápagos archipelago—a possibility thatweareexploringcurrently in thecoastalandagricultural zonesofotherislands.Moreover,urbaneffectsonfinchevolutionmightbecomparatively strong,given theirpersistence (continuedaccess tohumanfoods)asopposedtotheepisodicnatureofextremeclimaticevents.Our study also adds to the increasing evidence of humaneffectsonGalápagosbiodiversity.Thisincludesthenear‐extinctionof theMangrove finch resulting from the introduction of a para‐sitic fly (Fessl et al., 2010; Fessl,Dvorak,Vargas,&Young, 2011),andthecollapseofmultipleuniqueplantandanimalspeciesduetohabitatmodification,andtheintroductionandproliferationofalienspecies(Mauchamp,1997;Rentería,Gardener,Panetta,Atkinson,&Crawley,2012;Trueman,Atkinson,Guézou,&Wurm,2010;Watson,Trueman, Tufet, Henderson, & Atkinson, 2010).Our findings thusaccentuatethefragilityoftheinitialstagesofadaptiveradiationinDarwin’sfinchesandraiseconcernsaboutthefateoftheGalápagosecosystemsinthefaceofincreasingurbanizationandhumanpres‐ence. Ultimately, understanding the unexpected consequences ofurbanizationonecologicalnichesmightguidestrategiesforpreserv‐ingbiodiversityandtheprocessesthatgenerateit.

    ACKNOWLEDG EMENTS

    Logistical support and permits were provided by the GalápagosNational Park Service and the Charles Darwin Research Station.Funding was provided by the Earthwatch Institute in the formof a grant to LFD. Additional funding support was provided bySecretaríaNacionaldeCiencia,TecnologíaeInnovaciónandSistemaNacional de Investigación (LFD and DMTS), Sigma Xi (KMG), theNational Science and Engineering Research Council of CanadaVanier Scholarship (KMG), the European Society for EvolutionaryBiologyGodfreyHewittMobilityAward (KMG),McGillUniversity(KMG),andGAIAS‐USFQGrant(JAC).Wethanktheamazinggroupof Earthwatch volunteers who offered assistance in the field.Additional field assistancewas providedby S.Carvajal‐Endara,D.Hanson,andV.Vysna.

    CONFLIC T OF INTERE S T

    Nonedeclared.

    DATA ACCE SSIBILIT Y

    DataareavailableintheSupportingInformation.

    ORCID

    Luis F. De León http://orcid.org/0000‐0001‐9317‐420X

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