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Assymetric dispersal and colonization success of Amazonian plant-ant queens
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Title: Assymetric dispersal and colonization success of Amazonian plant-ant queens
Series Title: Bruna, E. M., T. Izzo, B. Inouye, M. Uriarte, & H. L. Vasconcelos. 2011. Assymetric dispersal and colonization success of Amazonian plant-ant queens. PLoS ONE 6(8): e22937
Physical Description: Journal Article
Creator: Bruna, Emilio
Publisher: Public Library of Science
Place of Publication: PLoS ONE
Publication Date: August 3, 2011
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Abstract: Background The dispersal ability of queens is central to understanding ant life-history evolution, and plays a fundamental role in ant population and community dynamics, the maintenance of genetic diversity, and the spread of invasive ants. In tropical ecosystems, species from over 40 genera of ants establish colonies in the stems, hollow thorns, or leaf pouches of specialized plants. However, little is known about the relative dispersal ability of queens competing for access to the same host plants. Methodology/Principal Findings We used empirical data and inverse modeling—a technique developed by plant ecologists to model seed dispersal—to quantify and compare the dispersal kernels of queens from three Amazonian ant species that compete for access to host-plants. We found that the modal colonization distance of queens varied 8-fold, with the generalist ant species (Crematogaster laevis) having a greater modal distance than two specialists (Pheidole minutula, Azteca sp.) that use the same host-plants. However, our results also suggest that queens of Azteca sp. have maximal distances that are four-sixteen times greater than those of its competitors. Conclusions/Significance We found large differences between ant species in both the modal and maximal distance ant queens disperse to find vacant seedlings used to found new colonies. These differences could result from interspecific differences in queen body size, and hence wing musculature, or because queens differ in their ability to identify potential host plants while in flight. Our results provide support for one of the necessary conditions underlying several of the hypothesized mechanisms promoting coexistence in tropical plant-ants. They also suggest that for some ant species limited dispersal capability could pose a significant barrier to the rescue of populations in isolated forest fragments. Finally, we demonstrate that inverse models parameterized with field data are an excellent means of quantifying the dispersal of ant queens.
Acquisition: Collected for University of Florida's Institutional Repository by the UFIR Self-Submittal tool. Submitted by Emilio Bruna.
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AsymmetricDispersalandColonizationSuccessof AmazonianPlant-AntsQueensEmilioM.Bruna1,6* ,ThiagoJ.Izzo2,6,BrianD.Inouye3,6,MariaUriarte4,6,HeraldoL.Vasconcelos5,61 DepartmentofWildlifeEcologyandConservationandCenterforLatinAmericanStudies,UniversityofFlorida,Gainesville,Florida,UnitedStates ofAmerica, 2 DepartamentodeBota ˆ nicaeEcologia,UniversidadeFederaldeMatoGrosso,Cuiaba ,MatoGrosso,Brazil, 3 DepartmentofBiologicalScience,FloridaStateUniversity, Tallahassee,Florida,UnitedStatesofAmerica, 4 DepartmentofEcology,EvolutionandEnvironmentalBiology,ColumbiaUniversity,NewYork,NewYork,UnitedStatesof America, 5 InstitutodeBiologia,UniversidadeFederaldeUberla ˆ ndia,Uberla ˆ ndia,MinasGerais,Brazil, 6 BiologicalDynamicsofForestFragmentsProject,InstitutoNacional dePesquisasdaAmazo ˆ nia&SmithsonianTropicalResearchInstitute,Manaus,Amazonas,BrazilAbstractBackground:Thedispersalabilityofqueensiscentraltounderstandingantlife-historyevolution,andplaysafundamental roleinantpopulationandcommunitydynamics,themaintenanceofgeneticdiversity,andthespreadofinvasiveants.In tropicalecosystems,speciesfromover40generaofantsestablishcoloniesinthestems,hollowthorns,orleafpouchesof specializedplants.However,littleisknownabouttherelativedispersalabilityofqueenscompetingforaccesstothesame hostplants.Methodology/PrincipalFindings:Weusedempiricaldataandinversemodeling—atechniquedevelopedbyplant ecologiststomodelseeddispersal—toquantifyandcomparethedispersalkernelsofqueensfromthreeAmazonianant speciesthatcompeteforaccesstohost-plants.Wefoundthatthemodalcolonizationdistanceofqueensvaried8-fold,with thegeneralistantspecies( Crematogasterlaevis )havingagreatermodaldistancethantwospecialists( Pheidoleminutula Azteca sp.)thatusethesamehost-plants.However,ourresultsalsosuggestthatqueensof Azteca sp.havemaximal distancesthatarefour-sixteentimesgreaterthanthoseofitscompetitors.Conclusions/Significance:Wefoundlargedifferencesbetweenantspeciesinboththemodalandmaximaldistanceant queensdispersetofindvacantseedlingsusedtofoundnewcolonies.Thesedifferencescouldresultfrominterspecific differencesinqueenbodysize,andhencewingmusculature,orbecausequeensdifferintheirabilitytoidentifypotential hostplantswhileinflight.Ourresultsprovidesupportforoneofthenecessaryconditionsunderlyingseveralofthe hypothesizedmechanismspromotingcoexistenceintropicalplant-ants.Theyalsosuggestthatforsomeantspecieslimited dispersalcapabilitycouldposeasignificantbarriertotherescueofpopulationsinisolatedforestfragments.Finally,we demonstratethatinversemodelsparameterizedwithfielddataareanexcellentmeansofquantifyingthedispersalofant queens.Citation: BrunaEM,IzzoTJ,InouyeBD,UriarteM,VasconcelosHL(2011)AsymmetricDispersalandColonizationSuccessofAmazonianPlant-AntsQueens.PLoS ONE6(8):e22937.doi:10.1371/journal.pone.0022937 Editor: WayneM.Getz,UniversityofCalifornia,Berkeley,UnitedStatesofAmerica Received February22,2011; Accepted July8,2011; Published August3,2011 Copyright: 2011Brunaetal.Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense,whichpermits unrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited. Funding: ThisresearchwassupportedbyGrantsDEB-0453631andDEB-0452720fromtheUSNationalScienceFoundation(http://nsf.gov).Publicationofthis articlewasfundedinpartbytheUniversityofFloridaOpen-AccessPublishingFund.Thefundershadnoroleinstudydesign,datacollectionandanaly sis,decision topublish,orpreparationofthemanuscript. CompetingInterests: Theauthorshavedeclaredthatnocompetinginterestsexist. *E-mail:embruna@ufl.eduIntroductionTheapproximately14,000speciesofants(familyFormicidae) accountforroughlyone-thirdoftheworld’sinsectbiomass[1]. Thedispersalabilityoffoundressqueensiscentraltounderstandingantlife-historyevolution,andalsoplaysafundamentalrolein antpopulationandcommunitydynamics,themaintenanceof geneticdiversity,andthespreadofinvasiveantspecies[2,3,4,5]. However,withtheexceptionofafewwell-studiedspecies[5,6], littleisknownregardingthedistancesqueenstypicallydisperse whentheyleavetheircoloniestofoundnewnestsorthemaximum distancestheyarecapableofdispersing(butseee.g.,[4,7,8]).This isbecausetechniquescommonlyusedtotrackdispersinganimals (e.g.,mark-recapturemethods,radiotransmitters)arerarely applicabletoantsgiventheirsize,thestructuralcomplexityof thehabitatthroughwhichtheydisperse,andthedifficultyin identifyingandsurveyingallpotentialnestingsites.Though genetictechniquesforestimatingdispersalappearpromising[4,8], theirapplicationmaybelimitedowingtotheirstringent assumptionsandchallengesinsamplingintensivelyenoughto accuratelyestimatedispersal. Thedominanceofantsisparticularlypronouncedinthetropics, whereinadditiontotheirnumericalsuperioritytheyarecritical predators,herbivores,ecosystemengineers,andagriculturalpests [1].Speciesfromatleast40generaoftropicalantsalsoestablish coloniesinthespecializedstems,hollowthorns,leafpouches,or petiolesofplantsknownas‘myrmecophyes’;theseantsdefend host-plantsagainstherbivoresandpruneencroachingvegetation [9,10].Multipleantspeciesoftenvieforthesamespeciesofhostplant[11,12],andvacantplantsinwhichqueenscanestablish PLoSONE|www.plosone.org1August2011|Volume6|Issue8|e22937

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coloniesarealimitingresourceforwhichthereisintense competition[13,14,15].Theorysuggeststhatinterspecificdifferencesinthedispersalcapabilityofantqueensplayakeyroleinthe maintenanceofdiversityinthesecommunities,eitherviatradeoffs betweendispersalabilityandotherlife-historytraits(e.g., competitiveability,colonyfecundity),orfromtheinteractionof dispersallimitationwithspatialheterogeneityinhost-plantdensity (reviewedin[3]).Studiesinmultipleplant-antsystemshave demonstratedinequitiesinthecompetitiveabilityofantqueensor colonies[16,17],plantandcolonydistributionconsistentwith habitatpartitioningandpatchdynamics[18,19],andpatternsof colonizationthatimplydispersallimitation[8,12,20]orinterspecificvariationindispersalability[20,21].Nevertheless,drawing generalconclusionsregardingtheimportanceofdispersalfor plant-antcoexistencerequiresquantitativedescriptionsofdispersal formultipleantscompetingforaccesstothesamehost-plants. Thebiologyofmyrmecophytesprovidesauniqueopportunity tocircumventthechallengesassociatedwithquantifyingantqueen dispersalinothersystems.Theantspeciesthatnestintheseplants dosoobligately,andeachisassociatedwithalimitedsubsetof plantspecies[11].Consequently,allantcoloniesinasite,aswell asallnestingsitestowhichqueenscouldpotentiallydisperse,can bereadilyidentifiedbymappingthedistributionofhostplants [8,22].Wemappedallindividualsoftheunderstoryshrubs Maieta guianensis and Tococabullifera (bothMelastomataceae)in9hectares ofprimaryforestinthecentralAmazon(Figure1).Thesetwo plantspeciesserveashostsforthreespeciesofantsymbiontsthat nestexclusivelyintheirdomatia: Crematogasterlaevis Pheidole minutula ,andanundescribedspeciesof Azteca [11,18,22]. Crematogasterlaevis competesforaccesstohostplantswithboth Azteca sp.and P.minutula (Figure2),andithasbeenhypothesized [21]thatsuperiordispersalabilitypromotesitspersistenceinthis systemdespitetheinferiorcompetitiveabilityofqueenscompeting foraccesstohost-plantseedlings[16],thepoordefensecolonies provideshost-plantsagainstherbivores[23],itslowratesofcolony persistence[18],andthehighmortalityratesofthehostplantsit occupies[18].Aftermappingallcoloniesofthethreeantspecies, wetransplantedvacant,greenhouse-grownseedlingsoftheirhost plants(N=50individualsofeachspecies)intothecentralhectare oftheplotandrepeatedlysurveyedthemforcolonizationbyant queens(seeMaterialsandMethods).Thesedata,coupledwiththe locationandsizeofestablishedcolonies,allowedustoestimatea probabilitydensityfunctiondescribingthespatialredistributionof successfullydispersingqueens(i.e.,the‘dispersalkernel’)ofeach antspeciesusing‘inversemodeling’–atechniquedevelopedby plantecologiststoestimatethedistancesseedsaredispersedfrom fruitingtrees[24,25,26].Toourknowledgethisisthefirst applicationofinversemodelingtechniquestocalculatethe dispersalkernelsofanimals.ResultsThemediandistancefromcolonizedseedlingstothenearest potentiallyreproductivecolonywassignificantlydifferentamong antspecies(Kruskal-Wallis,H=13.96,df=2, p 0.001,Figure3); experimentallytransplantedvacantseedlings(hereafter,‘‘trap plants’’,analogoustoseedtrapsusedinplantecology)colonized by Crematogatserlaevis queensweresignificantlyfurtherfrom reproductivecoloniesthanthosetrapplantscolonizedbyqueens ofeither Azteca sp.or Pheidoleminutula (Steele’sNonparametric MultipleComparisonTest[27],Table1).However,thisisnot becauseestablished C.laevis colonieswerelocatedfurtherfrom trapplants.Therewasasignificantdifferenceamongcoloniesof thedifferentspeciesintheirproximitytotrapplants(Table2),but P.minutula colonieswereactuallyfurtherfromtrapplantsthan thoseof C.laevis (averagedistancesfromtrapplantstocolonies: Figure1.Mapofestablishedantcoloniesandtargetseedlings. Locationandsizeofplantshostingcoloniesof Azteca sp., Crematogaster laevis ,and Pheidoleminutula andthelocationofexperimentallyplantedseedlings(‘‘trapplants’’)of Maietaguianensis and Tococabullifera doi:10.1371/journal.pone.0022937.g001 DispersalofAntQueensinTropicalForests PLoSONE|www.plosone.org2August2011|Volume6|Issue8|e22937

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Azteca sp.:116.09m 6 59.84SD, C.laevis :130.88m 6 60.60SD, P. minutula :137.59m 6 53.69SD,Figure4).Instead,ourinverse modelssuggest C.laevis queensestablishcoloniesfurthestfrom natalcolonies.Assumingalog-normalkernel(seeMaterialsand Methods),themodaldispersalandcolonizationdistanceof Crematogasterlaevis queensisdoublethatof Pheidoleminutula queens (40.1mand18.9m,respectively)andeight-foldthatof Azteca sp. (5m;Table3,Figure5).Thekernelsalsohadverydifferentshapes (Figure5),suggestingthatthemaximalcolonizationdistanceof C.laevis isapproximately80m,whilequeensof Azteca sp.maybe capableofinfrequentmovementsinexcessof400m.DiscussionWewereabletoestimatetheshapesofeffectivedispersalkernals forqueensofthreeantspecies.Thedispersalkernelfor Crematogasterlaevis hadthegreatestmode,suggestingthatit generallydispersesfurtherthaneitherantspecieswithwhichit competesforaccesstohostplants.However,ourresultsalso revealedthepotentialforlong-distancedispersaleventsby Azteca sp.Thatpotentialpartnerantspeciesdiffersignificantlyintheir capacitytodispersetoandcolonizehost-plantsplantsmayhelp explainpatternsofcolonizationandantcolonydistribution previouslyobservedinthis[18]andother[19,28,29]ant-plant systems.Alongwiththelackofspecializedentrancestodomatia (i.e.,‘‘lock-and-key’’mechanisms,sensu[30]),interspecificdifferencesindispersalandcolonizationsuccessmayalsobeimportant mechanismsinhibitingtheevolutionoffurtherspecializationin ant-plantsystems,inwhichthereareoftenlargedifferencesinthe qualityofdefenseandhostplantfitnessassociatedwithdifferent antpartnerspecies[18,23,31,32]. Ithaspreviouslybeensuggested[21]thatsmallerbodysize,and henceflightmuscles,mayexplainwhythe Pheidoleminutula queens havelowerdispersaldistancesthanthoseof Crematogasterlaevis ;the sameappearstobetrueinotherant-plantsystems[20].However, the Azteca sp.queenshavethelowestmodaldispersaldistanceof thesethreespecies,despitebeingsimilarinsizeto C.laevis .Given thepotentialforlongdistancedispersalbyqueensof Azteca sp.,we hypothesizethatthisshortermodaldispersaldistanceinstead Figure2.Focalcommunityofant-plantmutualists. Graphical depictionoftheAmazonianplant-antcommunityusedtoquantify dispersalcapabilityofantqueens.Valuesbyarrowsarethepercentage ofhost-plantscolonizedbyeachspeciesofantinour9-hastudysite. doi:10.1371/journal.pone.0022937.g002 Figure3.Distancefromcolonizedseedlingstothenearestreproductiveantcolony. Histogramsofthepairwisedistancesfromeach colonizedtrapplanttothenearestreproductivecolonyoftheantspeciesthatcolonizedit.A) Pheidoleminutula :meanpairwise distance=10.91m 6 5.26SD,B) Crematogasterlaevis :meanpairwisedistance=37.49m 6 25.92SD,C) Azteca sp.:meanpairwisedistance=12.30m 6 6.53SD. doi:10.1371/journal.pone.0022937.g003 DispersalofAntQueensinTropicalForests PLoSONE|www.plosone.org3August2011|Volume6|Issue8|e22937

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reflectstheirsuperiorefficiencyatfindinghostplants.Testingthis hypothesiswillbechallenging–itremainsamysteryhowplantantqueensinflightidentifyhost-plantseedlingsagainstabackdrop ofhundredsofotherplantspecies[9,33].However,itislikelythey useacombinationofvisualandolfactorycues,asisthecasewith phytophagousinsects[34].Indeedatshortdistances,queenshave beenshowntousevolatilesemittedbyplantstodiscriminatehostplantsfromcloselyrelatedbutnon-myrmecophyticspecies [33,35,36].Itmaybethat Azteca sp.queenshavetheabilityto detectthesevolatilesatgreaterdistancesthantheircompetitors, superiorabilitiestoidentifytheshapeofplantsandthe characteristicvenationpatternsofhost-plantleaves,orboth. Itisnotablethatthemodalantqueendispersaldistanceswe estimatedwithinversemodelsareshorterthantheaverage distancesinferredusingothertechniques[4,8,20]andwellbelow thepotentialdispersalcapacitysuggestedbyobservationsofantsin novelorexperimentallycreatedhabitatpatches[5,7].Ifhostplant densityisgreaterinoursitesthaninothersystems,thenqueens mightonlyberequiredtodisperseshortdistancestofindvacant hostplants.Amorelikelyexplanation,however,isthatprevious studieshaveoverestimateddispersal.Thiscouldresultfromnot exhaustivelymappingallpotentialsourceanddestinationhostplantsinasite[8,20],therebymissingmanyshort-distance dispersalevents. Ourstudyhastwoimportantcaveats.First,itwasconducted entirelyduringathreemonthperiodduringthedryseason.Little isknownregardingtheenvironmentalcuesthatstimulatethe nuptialflightsofantqueensintropicalforests[37],butthe colonizationofseedlingsby Pheidoleminutula inourfieldsites appearstobecloselylinkedtoprecipitation([21];seealso[37]for evidencefromPeruofsimilarseasonalityincolonizationof Cordia by Allomerusoctoarticulatus ).Ifthisseasonalvariationinhostplant colonizationby P.minutula iscommon,thencautionshouldbe takeninestimatingthetotalnumberofcolonizationsperyear usingourdata.Second,wecouldbeoverestimatingdispersal distancesforallthreespeciesifqueensarriveatexperimental seedlingsbutleftwithoutattemptingtocolonizethemordiedprior toenteringdomatia.Thelowdensityofvacantplants[15,22] probablymakesitextremelycostlyforaqueentodisperseagain onceshehasarrivedatahost-plantseedling,andextensivefield observationsindicatethatuponarrivingataseedlingqueensofall threefocaltaxaimmediatelyshedtheirwingsandattempttoenter domatia(HLVandTJI, personalobservation ).Somequeenswill probablydiepriortocolonizingtheseedlingonwhichtheyland, however,andthereissomeexperimentalevidencethat P.minutula successfullyentersdomatiaatahigherratethan C.laevis [16].Itis thereforepossiblethatusingcolonizationoftrap-plantsbyqueens asaproxyfordispersalmeansthatourresultsareconservative estimatestruedispersalability,especiallyfor C.laevis .Ifso,our estimatesofdispersalmightbestbecalled‘realizeddispersal’,i.e., dispersalfollowedbysuccessfulcolonization[8,20]. Inconclusion,ourresultshaveimplicationsforthestudyof plant-antdiversityintropicalecosystems.First,tropicalforestsare increasinglyfragmentedbyhumanactivities,whichisolates populationsofant-plantpartners[22].Thematingsystemof socialinsectsmakesthemparticularlysusceptibletoinbreeding [38],andisolatedpopulationsarefrequentlysmallerthanthosein unbrokenforest[22].Ifthedistanceseparatingfragmentsprovesa barriertodispersalforqueensofsomespecies,thiswillincreasethe likelihoodthatisolatedpopulationsofantsandtheirhost-plants couldsufferthedetrimentaleffectsofdemographic,environmental,orgeneticstochasticity[8].Second,acriticalbutrarely documentedrequirementofsomemechanismsthatpromote coexistenceinant-plantcommunitiesisthatpoorercompetitorsor habitatspecialistsaresuperiordispersers.Ourresultsare consistentwiththishypothesis,butalsosuggestthatattempting tocategorizespeciesas‘‘good’’or‘‘poor’’disperserswhentesting modelsofcompetition-colonizationtradeoffsisoverlysimplistic– isthebestdispersertheonethathasthegreatestpotentialdispersal distanceortheonethatdispersersfurtheronaverage?Finally,we showthataninversemodelingapproachcanhelpovercomethe challengesinquantifyingantdispersalinstructurallycomplex habitats,nottheleastofwhichisthedifficultyindocumentingrare long-distancedispersalevents[26].MaterialsandMethods EthicsStatementAllresearchwasconductedwiththeapprovalofBrazil’s NationalCouncilofScientificandTechnologicalDevelopment (CNPq,PermitNumber276/2005)andtheBrazilianInstituteof EnvironmentandRenewableNaturalResources(IBAMA,Permit Number226/2005).FieldSiteanddatacollectionFieldworkwasconductedJanuary–September2007inReserve # 1501oftheBiologicalDynamicsofForestFragmentsProject (BDFFP).This1,000hareserveislocated70kmnorthofManaus, Brazil(2 u 30 9 S,60 u W)andisembeddedinalarge( 10,000ha) expanseofprimaryforest.Thehabitatisnon-floodedlowlandrain forest,witha30–35mtallcanopyandanunderstorydominated bystemlesspalms.Soilsinthesitesarehighlyacidicandnutrient poorxanthicfarralsolswithpoorwaterretentioncapacity[39]. Annualrainfallrangesfrom1,900–3,500mmperyear,andthere isapronounceddryseasonfromJune–October[40]. Tococabullifera (Melastomataceae)isanunderstoryshrubthat growstoamaximumheightof2–3m.Ithastwopouchesatthe baseofeachleafinwhichantqueensestablishcolonies[18,41]. Table1. ResultofSteel’sTestcomparingthemedian distanceofcolonizedtrapplantstothenearestreproductive colonyforallpairwisecomparisonsofantspecies. Comparison RelativeEffect, ^ p p (lower-upper95%confidencelimits) pvalue Azteca sp.vs. Crematogasterlaevis 0.82(0.58–1.07)0.005 Azteca sp.vs. Pheidole minutula 0.45(0.21–0.68)0.87 C.laevis vs. P.minutula 0.15( 2 0.09–0.40)0.002 doi:10.1371/journal.pone.0022937.t001 Table2. NestedAnalysisofVariancecomparingtheaverage distanceoftrapplantstocoloniesofthethreeantspecies ( Crematogasterlaevis Azteca sp., Pheidoleminutula )mapped inour9hastudysite. Source df MS F PAntSpecies2496230169.68 0.0001 Trap(AntSpecies)3740.0250.99 Error1669448822953 (NestedANOVA;MaineffectofAntspecies:F2,16694=169.68,P= 0.0001). doi:10.1371/journal.pone.0022937.t002 DispersalofAntQueensinTropicalForests PLoSONE|www.plosone.org4August2011|Volume6|Issue8|e22937

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Maietaguianensis (Melastomataceae),alsoanunderstoryshrub, growstoaheightof1.5m[18,21].Ithashighlydimorphicpaired leaves,withapairoffoliarpouchesatthebaseofthelargerleaves inwhichantsnest.Inourstudysitestwoantspeciesareassociated with M.guianensis ;mostplantscontaincoloniesof Pheidoleminutula (95%),withtheremainderoccupiedby Crematogasterlaevis (5%). Theantassociatesof T.bullifera areanundescribedspeciesof Azteca (67%)and Crematogasterlaevis ( 33%)(Figure2).These frequenciesaresimilartothosereportedinprevioussurveys conductedinourfieldsites[18].Althoughapreviousstudy conductedinourstudysites[11]hastreatedthe Azteca speciesthat colonizes T.bullifera and M.guianensis asthesameonecolonizing thesympatricmyrmecophyte Cordianodosa (Boraginaceae),this appearstobeamisidentificationresultingfromtheuseofworker morphologytodifferentiatespecies.Thecomplextaxonomyof Azteca requiresusingqueenstodistinguishspecies[42];differences between Azteca queensfrom C.nodosa andthosefrom T.bullifera in size,coloration,theshapeofthepropodeum,andthenumberof propodealhairsstronglysuggestthesearedistinctspecies(T.Izzo, unpubl.data ).Althoughseedlingsofbothplantspeciescanharbor incipient(i.e.,non-reproductive)coloniesofmorethanoneant species,adultplantshousejustasinglecolonyofonlyonespecies. Inadditiontoscavengingforinsectsontheleafsurface,resident antstendcoccidsforhoneydewinsidedomatia[43,44]. Figure4.Pairwisedistancesfromestablishedcoloniestotrapplants. Histogramsofthedistancefromtrapplantstocoloniesforeachofthe threefocalantspecies.TheXaxisshowsthepercentageofallcolony-trappairwisecomparisons.A) Pheidoleminutula :meancolony-trap distance=137.59m 6 53.69SD,B) Crematogasterlaevis :meancolony-trapdistance=130.88m 6 60.60SD,C) Azteca sp.:meancolony-trap distance=116.09m 6 59.84SD. doi:10.1371/journal.pone.0022937.g004 Table3. Maximum-likelihoodparameterestimates(MLE)and95%supportintervals(SI)forinversemodelsestimatingthe dispersalkernelsofthreemutualistantspeciesnestingintwospeciesofAmazonianant-plants.PheidoleminutulaAztecasp.Crematogasterlaevis Parameter1MLE (lowerSI-UpperSI)MLE (lowerSI-UpperSI)MLE (lowerSI-UpperSI) X018.85(17.42–20.47)5(5–5.05)40.16(31.54–52.16) Xb0.14(0.09–0.23)1.85(1.21–1.93)0.27(0.15–0.66) a 1.58(1.00–4.00)11.40(7.45–22.57)14.84(8.75–23.36) b 55.07(36.50–96.20)114.15( 2 10.00–250.00)1.91(0–10)1Parameters: X0=Modeofthelog-normaldispersalkernel, Xb=Varianceofthelog-normaldispersalkernel, a =Slopeofthelinedescribingtherelationshipbetween plantsizeandqueenproduction, b =Interceptoftherelationshipbetweenplantsizeandqueenproduction. doi:10.1371/journal.pone.0022937.t003 DispersalofAntQueensinTropicalForests PLoSONE|www.plosone.org5August2011|Volume6|Issue8|e22937

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FromJanuary–July2007wedemarcateda9-haplotatreserve 1501andthenmarkedandmappedall Maietaguianensis and Tococa bullifera intheplot(Figure1).Foreachplantwerecordedthe identityofitsantresidentestimateditssizebycountingthe numberofdomatiabearingleaves.Wemappedatotalof217 M. guianensis ( n =10with Crematogasterlaevis colonies, n =207with Pheidoleminutula colonies)and79 Tococabullifera ( n =26with C.laevis colonies, n =53with Azteca sp.colonies). BecausecolonysizeinAmazonianplant-antsislimitedbythe numberofhost-plantdomatia[15],weuseddomatianumberasa proxyforcolonysize.Toestimatequeenproductionasafunctionof colonysizewedestructivelysampled67 Tococabullifera with Crematogasterlaevis n =83 T.bullifera with Azteca sp., n =87 Maieta guienensis with C.laevis and n =101 M.guianensis with Pheidoleminutula allfromnearbylocationsoutsideoft hefocalstudyarea.Ofthese,9,9, 11,and36colonies(respectively),werereproductive.Weusedthese reproductivecoloniestoestimatetherelationshipbetweencolonysize andqueenproduction(Table4);linearregressionprovidedabetterfit tothedatathannon-linearmodels( resultsnotshown ). Wethenestablishedanarrayofgreenhouse-grownseedlingsin thecenterofthe9-haplot(Figure1).Thearraywascomposedof n =50 M.guianensis (forcolonizationby Pheidoleminutula or Crematogasterlaevis )and n =50 T.bullifera (forcolonizationby Azteca sp.or C.laevis ).Seedlingshadatleasttwofullyexpandedleaves withdomatiaandwerearrangedinagridwithspeciesalternating andplantsseparatedfromeachotherby10m.Seedlingsof T. bullifera weregrownfromseedscollectedinReserve1501and germinatedinashadehouseinmoistsand;becauseofthe difficultyingerminating M.guianensis seedswecollectedvacant M. guianensis seedlingsinthereserveandtransplantedthemto containersfilledwithlocalsoilandmaintainedinthesame shade-house.FromJuly–September2007wesurveyedthetarget Figure5.DispersalkernelsforthreespeciesofAmazonianplant-ants. Dispersalkernels(i.e.,probabilitydensityfunctionsdescribingthe spatialredistributionofqueensaroundreproductivecolonies)forantqueensobligatelynestingin Tococabullifera or Maietaguianensis .Thesekernels arescaledforacolonyhousedinaplantofthemediansizeobservedinour9-hastudyplot. doi:10.1371/journal.pone.0022937.g005 Table4. Resultsoflinearregressionstestingforarelationshipbetweenthenumberofdomatiaaplanthasandthenumberof queenscountedinthataplant. Antspecies Hostplant df SS SS Fvalue Pvalue R2 Regressionequation (regression) (residual) CrematogasterlaevisMaietaguianensis 1,1018.432.5771.651 0.00010.88 queens p ~ 0 : 404 domatia p PheidoleminutulaMaietaguianensis 1,35228.5440.46197.72 0.00010.85 queens p ~ 0 : 726 domatia p Azteca sp. Tococabullifera 1,830.913.0980.09 0.00010.91 queens p ~ 0 : 333 domatia p CrematogasterlaevisTococabullifera 1,8120.2694.7210.160.0130.56 queens p ~ 1 : 242 domatia p Notethattheinterceptofallthreeregressionsiszerobecausequeensareonlyfoundinplantswithatleastonedomatium. doi:10.1371/journal.pone.0022937.t004 DispersalofAntQueensinTropicalForests PLoSONE|www.plosone.org6August2011|Volume6|Issue8|e22937

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seedlings15,35,and90daysaftertransplantingtorecordthe presenceandspeciesidentityofqueens.Allqueensfoundwere removedtoallowforsubsequentcolonization,whichprevious workhasshowndoesnotinfluencetheprobabilityofrecolonization[21].Therewere n =17colonizationsby C.laevis n =23by Azteca sp.,and n =25by P.minutula Crematogasterlaevis colonized n =15ofits100potentialhostplantseedlings(15%), while Pheidoleminutula colonized n =17outof50(34%)and Azteca sp.colonized n =17outof50(34%),whiletheremainingevents wererepeatcolonizationsofindividualseedlings.ModelingframeworkWeusedinversemodels[26,45]parameterizedwiththe observationalandexperimentaldatadescribedabovetocharacterize thecolonizationofhostplantsbyqueensofourthreefocalspecies. Thismethodassumesthatobserveds patialvariationincolonization ofhostplantsbyqueensisamultiplicativefunctionofqueen production,whichisbasedonthesizeofpotentialqueensources(i.e., host-plantsize),andlocaldispersal,whichismodeledwithadispersal kernelthataccountsforproximityofthesourcestoexperimentalhost seedlings.Forthoroughreviewsofinversemodelsandtheir construction,assumptions,andapplicationsee[24,26,45]. Thetotalnumberofdispersingqueens, t ,producedbyacolony wasestimatedasalinearfunctionofthenumberofdomatiaits hostplanthasasfollows: t ~ a domatia z b 1 wheretheparameter a determinesthesteepnessintheincreasein queenproductionwiththenumberofdomatia,and b determines theinterceptofthedomatia-queenproductionrelationship. Weusedalognormaldispersalfunction,whichconsiderable empiricalandtheoreticalworkhasfoundtobethemostappropriate functionforavarietyofdispersalmechanismsincludinganimal movement([46,47,48,49],reviewedin22).Thekerneltakestheform: f ( d ) ~ 1 g e{ 1 2 ln d = X0 Xb0 @ 1 A2 2 where d istheobserveddistancebetweenthecolonyandthe vacanthostplantseedling, X0isthedistanceatwhichmaximum recruitmentoccurs(i.e.,themodeofthedispersalkernel), Xbdeterminesthebreadthorspreadofthedispersalkernel,and g isa normalizationconstantequaltothearcwiseintegrationofthe dispersalkernel[25]. Combininglocalqueenproduction Q andthedispersalkernel resultsinamodelforthepotentialnumberofqueensintrapplant i overthecourseofoursamplinginterval: Qi~ Xn k ~ 1 a tk1 z ( a = b ) tkf ( dik) 3 where tkisthenumberofqueensof k =1… n colonieswithinthe maximaldispersaldistance(inmeters)suggestedbyourmodelin the9haplot, dikisthedistancefromhostplant i tosourceplant k and f() isthelognormaldispersalkernel.Forallanalyseswe assumedthattheexpecteddensityofqueensinahostplantfollows anegativebinomialdistribution,reflectingthehighdegreeof clumpingobservedinthedata[50].Weusedsimulatedannealing, aglobaloptimizationalgorithm,tofindtheparametervaluesthat maximizedthelikelihoodofobservedrecruitmentdensities.We alsocalculatedasymptotic95%supportlimitsforallthe parameters.TheseAnalyseswereconductedusingRv2.9.2 statisticalsoftware[51]andthepackages‘‘Likelihood1.3’’and ‘‘NeighLikeli1.0’’,aswereallstatisticalanalyses.AcknowledgmentsWethankScottPowell,W.Getz,andthreeanonymousreviewersfor commentsonthemanuscriptandEmiliaZoppasdeAlbuquerque,Wesley Da ttiloandOsmaildoFerreiradaSilvaforassistanceinthefield.The BDFFPstaffprovidedinvaluablelogisticalhelp;thisispublication582in theBDFFPtechnicalseries.Datausedinthispaperhavebeenarchivedat Dryad(www.datadryad.org):doi:10.5061/dryad.h6t7g.AuthorContributionsConceivedanddesignedtheexperiments:EMBBDIHLVTJI.Performed theexperiments:TJI.Analyzedthedata:EMBMUBDIHLVTJI. 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