International Master Programme at the Swedish Biodiversity Centre

Master theses No. 41 Uppsala 2007 ISSN: 1653-834X Effects of landscape pattern and resource distribution on frugivorous bird species in the central andes of colombia: setting ecological thresholds

Javier Eduardo Mendoza S. Supervisors Johnny de Jong Gustavo H. Kattan MASTER SERIES THESES MASTER SERIES THESES MASTER SERIES THESES MASTER SERIES THESES CBM CBM CBM CBM Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

CBMMasterThesesNo.41 1 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Abstract Understandingwildlifedistributionalpatternsandtheirrelationshipwith landscapecharacteristics(coverandconfiguration)andresourcedistributionis keyfortheirconservation,especiallyintransformedlandscapes.Theoretically, insomecasestherearethresholdvaluesinhabitatamountandconfiguration, belowwhichspeciespersistenceiscompromised.Ianalyzedtherelationshipof forestfrugivorousbirdspeciestothedistributionofkeyfruitingtrees( Cecropia, and Miconia )andlandscapecharacteristicsofforestpatchesatthree differentspatialscales,local(3ha),intermediate(312ha)andlandscape(2500 ha),intheCentralAndesofColombiatolookforindicationofstatistically significantecologicalthresholds(e.g.nonlinearrelationshipsbetweenspecies presenceandhabitat).Iuseddatafromfour2,500harurallandscapeswith differentfragmentationlevels(80%,46%,25%and20%forestcover)between 1700and2100monthewesternslopeoftheCentralAndes.Ingeneral,the distributionoffrugivorousbirdspecieswasbetterexplainedatlocaland intermediatescalesbylandscapecharacteristics,especiallyforestcover,than fruitresourcesdistribution.Atlocalscale,Iestablished27speciesspecific occurrencethresholdsinfourlandscapecharacteristicvariablesandinonefruit resourcesvariable,for13forestfrugivorousbirdspecies.Atintermediatescale Idetectnineoccurrencethresholdsintwolandscapecharacteristicvariables andonefruitresourcedistributionvariableforsevenbirdspecies.Atlandscape scale,notsignificantrelationshipswerefoundbecausewerenotenough replicates.Atlocalandintermediatescalesthespecieswhichexhibitingthe highestdiscriminationbetweenpresenceandabsencebasedonlandscape characteristicstoindicateecologicalthresholdswerelargebodiedfrugivorous. However,theirusemustbedonecarefullytoavoidmisinterpretationsin decisionmakingprocesseswhichcouldleadmajornegativeimplicationsfor conservation. Keywords:HabitatAmount,KeyFruitingTrees,LandscapeConfiguration, OccurrenceThresholds,ROCCurves,SpeciesDistribution.

CBMMasterThesesNo.41 2 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

CBMMasterThesesNo.41 3 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Contents Introduction - 6 - Study Area and Methods - 8 - Bird Survey - 9 - Trees Sampling - 10 - Results - 16 - Relationship between abundance and richness of birds and resources - 17 - Birds explanatory variables relationship - 17 - Ecological Thresholds - 23 - Discussion - 28 - Acknowledgments - 33 - References - 34 - Appendix 1 Species of Cecropia, Ficus and Miconia and their total abundance recorded in the study areas of the Central Andes of Colombia - 40 -

CBMMasterThesesNo.41 4 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

CBMMasterThesesNo.41 5 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Introduction Aslandusesincreaseinintensityandextensionitisimportanttounderstand theroleoflandscapepatterninpreserving,alteringoreliminatingbiological communities(Milleretal.1997).Theeffectsofhabitattransformationon wildlifedependsoninteractionbetweenthescaleatwhichtheorganisms functioninthelandscape,thepatternsofdistributionandabundanceof organismsinthelandscape,andhowtheyarealteredbyhabitattransformation (Kattan&Murcia2003).Understandingthesechangesandtheirconsequences onbiodiversityarerelevantissuesespeciallyinmegadiversecountrieswhere thedeforestationrateisincreasing. Foodabundancevariesthroughtimeandspace,butmaydirectlyinfluence abundanceoforganismspresent(Block&Brennan1993).Thedistributionof theseresourceswillconditionhabitatquality,resultinginsource–sink relationships(Pulliam1988)amongotherrelationships.Severetransformation causedbyhabitatlosscannegativelyaffectthedistributionalpatternsof resourcesespeciallyforcertainguildsasfrugivorousandinsectivorous(Sodhi etal.2004)andproducechangesinthecompositionofallspecies communities.Distributionoffrugivoresisimportantfortropicalforest conservation,becauselossofanimalmutualismslikelossofseed dispersingspecieswillpotentiallyhavelargeimpactsonpatternsofseed depositionandfuturedistributionandconservationofmanyplantspecies. Furthermore,lackofdisperserwillincreaselocalextinctionsofplantspecies (Groom1998;Amaraskare1998;Bodinetal.2006),especiallyofpopulations withlowdensities.Overtime,thesechangesmaycausesynergiceffectson communitystructureandfunctionofthenativeforests(Loiselle&Blake 2002). Certainplantgeneracouldbeconsideredaskeyspeciesforfrugivoresdueto thefactthattheyprovidefruitsnotonlyduringperiodsofhighabundanceof fruits,butalsoduringscarcityperiodsoffruits.InAndeanforests Cecropia (Cecropiaceae), Ficus ()and Miconia (Melastomataceae)aregenera withseveralspecies,notonlycharacteristicsfromopenareasandsecondary forestsbutalsofrominteriorhabitats(Vargas2002),andwithasynchronical phenologypatterns(Ríos2005;Ríos&Kattaninprep.;Valenzuela&Kattanin prep.).Thismeansthattheycouldbeconsideredaskeyresourcesfor frugivores,notonlybirdsbutalsoabroadvarietyoftaxa(Luck&Daily2003; Loiselle&Blake1999;Poulinetal.1999;Lambert&Marshall1991;Loiselle& Blake1990;Estradaetal.1984).However,onlythelocalhabitatconditions maybeinadequatetoexplainspeciespresenceorabundance;thesignificant effectofboundaryshapeorcharacteristicsofthesurroundinglandscapemust beconsidered(Turner2005),becausesomespeciesmightbefavoredmore thanothersintheirdistributionandalsotheycanaffectotherfunctionssuch asrelationshipsbetweenspecies(i.e.predator–preyinteractions).

CBMMasterThesesNo.41 6 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Studiesexploringtheeffectsoflandscapecontextandpatchcharacteristicsto establishrelationshipswiththestructureandcompositionoffaunal communitieshavebeenconductedfordifferenttaxaandlandscapetypes(see Mazerolle&Villard1999).Themostimportantlandscapecharacteristics influencingspeciesrichnessandabundancearepatchsize(MartinezMorales 2005;Corneliusetal.2000;AbenspergTraunetal.1996;Vos&Stumpel 1995),patchshape(MartinezMorales2005);edgeextentandnature(Watson etal.2004;Campi&MacNally2001;Restrepoetal.1999);landcoverand landscapeconfiguration(Bishop&Myers2005;Watsonetal.2005;Westphal etal.2003;Flather&Bevers2002;SteffanDewenteretal.2002;Trzcinskiet al.1999;McGarical&McComb1995;Villardetal.1999).Inmanycases,a singlestudyfoundsignificantrelationshipswithmorethanoneonthese characteristics.However,acommonprobleminmanystudiesisincorrect extrapolationsofresultsfromsmallscalestolargescales(McGarical& Cushman2002). Onetoolthathasbeensuggestedforassessingtheconsequencesoflandscape transformationissettingthresholdvaluesinecologicalprocesses(Fahrig2001; Hugget2005;Lindenmayeretal.2005;Radfordetal.2005).Ecological thresholdsarecriticalvaluesofanindependentvariablearoundwhichthe systemflipsfromonestatetoanother(Muradian2001).Thresholdshavebeen establishedusingbothempiricalandsimulationdata(Fahrig2002;Dykstra 2004).Examplesofthresholdvaluesare,extinctionthresholds(Tilmanetal. 1994;Fahrig2001,2002),fragmentationthresholds(Andrén1994,1999), connectivitythresholds(With&Crist1995;Metzger&Décamps1997;Schultz &Crone2005),andoccurrencethresholds(Hansenetal.1995;Bütler2004; Guénette&Villard2004,2005).Thresholdvaluescanprovideinformationto definesensitivityofspeciestoprocessesthatthreatenmanyecological processeshavingpotentialutilityinconservationandmanagement(Hugger 2005). InColombia,theAndeanregionhasahighvarietyofbiophysical environmentsdueitshightopographicalcomplexity.Thishasgeneratedgreat diversityandendemism,inalimitedspace(Etter&vanWyngaarden2000; Kattanetal.2004)reflectedinhighbetadiversityvaluesformanytaxasuchas birdsand(Kattanetal.2006;Mendozaetal.inprep.).However, historicallythisregionisoneofthemostfragmentedareasinthecountry becauseofthepopulationgrowthandthespreadingofcoffeecropsandcattle ranchingduringthefirstdecadesof20thCentury.Sincethen,majorityof forestpatchesareonprivatelandsandveryfewpolicyinstrumentshavebeen implementedtopromoteforestandspeciesconservationwithinthe landowners’community.Asaconsequenceofthislongtermforest fragmentation30%offorestbirdspeciesarecurrentlyextinctinsubAndean forests(Renjifo1999).Largebodiedcanopyfrugivoresandunderstory

CBMMasterThesesNo.41 7 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

insectivoresarethemostsensibleguildstohabitatfragmentationinthetropics (Kattanetal.1994;Kattan1992). Iinvestigatedthespecies/habitatrelationshipsusinglandscapecharacteristics andfruitresourcevariableswhicharesupposedtoinfluencetheforest frugivorousbirdspeciesassemblages.AlsoIinvestigatedagradientofhabitat transformationandfruitresourcedistributiontoexplorethresholdvaluesfor speciesoccurrence.ThequestionsIaddressedwere,(1)Howwelldoesthe abundanceanddistributionoffruitingtrees(gen. Cecropia, Ficus and Miconia ) explainthedistributionoffrugivorousbirdspecies?;(2)Howwelldolandscape variablesexplainthedistributionoffrugivorousbirdspecies?,and(3)Arethere ecologicalthresholdsforlandscapevariablesandabundanceanddistributionof fruitingtreesaffectingthefrugivorousbirddistribution?

Study Area and Methods Iconductedmystudyinfour2500harurallandscapeswithdifferentamounts ofnativeforest,between1700and2100m.a.s.l.onthewesternslopeofthe CentralAndesofColombia.Fromnorthtosouththeyare(Fig1):1)Mid ChamberyRiverwatershed(henceforthChambery)(75º30’5”W,5º16’34”N), MunicipalityofAranzazu,Caldas,with20%forestcover;2)OtúnRiver watershed(Otún)(75º33’8”W,4º42’43”N),MunicipalityofPereira,Risaralda, 80%ofnativeforestcover;3)BarbasRiverCanyon(Filandia)(75º35'42"W 4º40'48"N)MunicipalityofFilandia,Quindío,46%ofnativeforestcover;and 4)MidNimaRiverwatershed(Nima)(76º9’1”W,3º30’41”N),Municipalityof Palmira,ValledelCauca,25%forestcover.Alltheseareasarecharacterizedby SubAndeanforest,withmeanannualtemperatureandrainfallof19 oCand2 000to3000mm.Themainlandusesinalllandscapesarelivestockpastures andforestryplantationsofexoticspecies( Pinus, Cupressus and Eucalyptus ). In2002–2005theAlexandervonHumboldtInstitute(AvHI)conducted biodiversitycharacterizationsinthesameareawithintheProject “ConservationandsustainableuseofbiodiversityintheColombianAndes” (IAvH2007).Theselandscapeswereselectedinagreementwithregional authoritiesandlocalcommunitiesaccordingtotheirconservationpriorities, andbecausetheywereconsideredasrepresentativesamplesofsubAndean landscapeswithdifferentamountofnativeforesttoevaluatecontributionof differenthabitatstoregionaldiversityandpotentialeffectsofhabitatlossin speciesdiversity.Ineachlandscapedifferenthabitatsweresampled(native forest,grasslands,forestryplantationsandcrops).Samplingsiteswereselected accordingtotheirvegetalstructureaimingatarepresentativepictureofeach habitat.Withineachhabitatasamplingunitwaslocated,thiswascomposedby twobirdcountpointsandfourtransectsforvegetationsurvey(Fig.2).Intotal

CBMMasterThesesNo.41 8 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

138samplingunitsweremade(40inChambery;22inOtún;40inFilandiaand 36inNima)andspeciesrichnessandabundanceofbirds,treesandants(not consideredhere)specieswasrecorded. COLOMBIA 1 Caldas 1 Risaralda 2 3 2 Quindío 4 Valle del Cauca 3 4 Fig.1:MapofthestudyareaintheCentralAndesofColombia.1.MidChamberyRiver watershed(20%forestcover).2.MidOtúnRiverwatershed(80%).3.BarbasRiver Canyon(46%).4.MidNimaRiverwatershed(25%),Blackareasrepresentnativeforest landcover. Bird Survey Thesamplingmethodforbirdswaspointcounts(50mradius,twopereach site,equivalentto523,3m 2,separateoneeachother50mDailyetal.,2001) usingvisualobservationandvocalizationrecordingswithinthe50mradius. Eachsitewassampledforthreerepetitionsconsecutivedaysbetween06h00 and10h00during15minutes(exceptwindyorrainydays;Renjifo1999).The

CBMMasterThesesNo.41 9 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

combinationofmethodsattemptedtoconsiderdifferencesindetectability amongthespecies(Mendozaetal.inpress). Trees Sampling Fortreesdatafourtransects50x4m(800m 2)weremadeadjacenttoeachbird samplingsite.Becauseparalleltransectswerenotindependentonetoeach other(5m),fortheanalysisthedatafromtransectoneandthree,andtwoand fourwerepooled(Fig.2).Alltreeindividualswithdbh≥5cmwerecounted (Mendozaetal.inpress).

Radius 50 m Transects for trees 1th birds point sampling (DBH >5cm) count : 2th bird point observations and counts song recording 4m 1 2

0m 50m 100m 150m 5m ca. 3 4 Fig.2:Diagramofsamplingunitsforbirdsandtreesusedtodatarecordingbythe HumboldtInstitute(ModifiedfromMendozaetal.inpress). Fromthosedatabasesandbecausemyaimswererelatedtoforestspecies,I choseformystudyonlytheinformationfromnativeforesthabitats(n=76; distributed:16inChambery;16inOtún;20inFilandiaand24inNima)(Fig. 1),anddataofspeciesrichnessandabundanceofforestfrugivorousbird speciesand Ficus, Cecropia and Miconia trees.Intotal58birdspecies(excluding migratoryspecies),and33fruitingtreespecieswereselected(Table1, Appendix1).

CBMMasterThesesNo.41 10 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Table1:FrugivorousbirdspeciesrecordedinfourlandscapesofsubAndeanforestin CentralAndesofColombiaandtheirfrequencyofoccurrence.Inboldthespecieswhich metthecriterionsofabundance:speciesonlypresenton≥10%or≤90%ofthe76 sites;andthecriterionofareconsideredasnegativelyaffectedspeciesbyhabitat transformationaccordingtoDCAandCCAresults. Frequencyof AbbreviationAbbreviationScientificnameScientificname OccurrenceOccurrence LandscapeLandscape (mean(mean± ±±±SD)SD)SD)Chambery FilandiaFilandiaNimaNima OtúnOtún Aabur Aburria aburri (5.26±0.22) X X Amazona Amerc mercenaria (6.58±0.24) X X X Anisognathus Aflav flavinucha (30.26±0.46)(30.26±0.46) X X X X Awagl Aratinga wagleri (17.11±0.37)(17.11±0.37) X X Aulacorhynchus Ahaem haematopygus (52.63±0.50)(52.63±0.50) X X X X Aulacorhynchus Apras prasinus (35.53±0.48)(35.53±0.48) X X X X Bmont Buthraupis montana (2.63±0.16) X Chamaepetes Cgoud goudotii (19.74±0.40)(19.74±0.40) X X X Chlorochrysa Cniti nitidissima (3.95±0.19) X X Cspiz Chlorophanes spiza (6.58±0.24) X Chlorophonia Ccyan cyanea (1.32±0.11) X Chlorospingus Ccani canigularis (10.53±0.30)(10.53±0.30) X X X Chlorospingus Copht ophthalmicus (7.89±0.27) X X X X Cfasc Columba fasciata (17.11±0.37)(17.11±0.37) X X X Dalbi Diglossa albilatea (1.32±0.11) X Dcyan Diglossopis cyanea (1.32±0.11) X Ebour Eubucco bourcierii (31.58±0.46)(31.58±0.46) X X X Emusi Euphonia mumusicasica (34.21±0.47)(34.21±0.47) X X X X Euphonia Exant xanthogaster (36.84±0.48)(36.84±0.48) X X X Hcris Habia cristata (5.26±0.22) X X Hemispingus Hfron frontalis (1.32±0.11) X Hemispingus Hsupe superciliaris (22.37±0.41)(22.37±0.41) X X Hguir Hemithraupis guira (1.32±0.11) X Mchry Masius chrysopterus (6.58±0.24) X X Moliv Mionectes olivaceus (10.53±0.30)(10.53±0.30) X X X Mionectes Mstri striaticollis (10.53±0.30)(10.53±0.30) X X X Mrall Myadestes ralloides (78.95±0.41)(78.95±0.41) X X X X Myiodynastes Mychry chrysocephalus (42.11±(42.11±0.49)0.49)0.49) X X X X

CBMMasterThesesNo.41 11 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Omomo Ortalis motmot (28.95±0.45)(28.95±0.45) X X Ppiti Parula pitiayumi (67.11±0.47)(67.11±0.47) X X X X Ppers Penelope perspicax (17.11±0.37)(17.11±0.37) X X Pharomachrus Pauri auriceps (10.53±0.30)(10.53±0.30) X X X Pchal Pionus chalcopterus (17.11±0.37)(17.11±0.37) X X X Ptumu Pionus tumultuosus (6.58±0.24) X X Pipraeidea Pmela melanonota (11.84±0.32)(11.84±0.32) X X X Prief Pipreola riefferii (1.32±0.11) X Pleuc Piranga leucoptera (5.26±0.22) X Plleucs Platycichla leucops (1.32±0.11) X Pscut Pyroderus scutatus (15.79±0.36)(15.79±0.36) X X Ramphocelus Rflam flammigerus (10.53±0.30)(10.53±0.30) X X X Salbic Saltator albicollis (19.74±0.40)(19.74±0.40) X X X Satri Saltator atripennis (52.63±0.50)(52.63±0.50) X X X X Sericossypha Salbo albocristata (2.63±0.16) X Tarth Tangara arthus (61.84±(61.84±0.48)0.48)0.48) X X X X Tcyan Tangara cyanicollis (5.26±0.22) X X Tgyro Tangara gyrola (15.79±0.36)(15.79±0.36) X X X X Thein Tangara heinei (50±0.50)(50±0.50) X X X X Tangara Tlabr labradorides (5.26±0.22) X X Tnigr Tangara nigroviridis (9.21±0.29) X X X Tvasso Tangara vassori (1.32±0.11) X Tvitr Tangara vitriolina (38.16±0.48)(38.16±0.48) X X X X Tangara Txant xanthocephala (2.63±0.16) X X Tepis Thraupis episcopus (10.53±0.30)(10.53±0.30) X X X Tpalm Thraupis palmarum (5.26±0.22) X X Tfusc Turdus fuscater (14.47±(14.47±0.35)0.35)0.35) X X Tigno Turdus ignobilis (17.11±0.37)(17.11±0.37) X X X X Tserr Turdus serranus (2.63±0.16) X Zimmerius Zviri viridiflavus (90.79±0.29) X X X X Ievaluatedtherelationshipsbetweenfrugivorousbirdspeciestolandscape characteristicsandfruitresourcesdistribution,atthreeecologicalscales,local, intermediateandlandscape.Imeasuredthelandscapecharacteristicvariables (Table2)usingthelandcoverinterpretationsinvectorformatofeachstudy areaproducedbytheGISUnitoftheAvHI.Togeneratethosemapsaerial photographs(scale1:25000;yrs.1986and1990)andQuickBirdsatellite images(1mresolution,yrs.2002and2003)wereused.Atlocalscale,Imadea bufferringwith100mradiusovereachsamplingpointtousethesameareato measuretheexplanatoryvariables(Table2),76unitswereconsidered.For

CBMMasterThesesNo.41 12 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

intermediatescale,eachlandscapewasdividedineightquadrants(312ha), having32units.Forlandscapescalewasthe2500hawindow(n=4). Becausesomesamplingpointswhichareclosertogetherhaveatendencytobe moresimilarthatthingsthatarefartherapart,isalackofindependenceamong observationscreatingspatialautocorrelation(SA)(Dale&Fortin2002). Spatialautocorrelationcreatesapparentlysignificantresultsmoreoftenthanin fullyindependentdata.Then,beforethestatisticaltestsarerunning,the magnitudeandstructureofSAneedstobedeterminate.Ifoundsignificant spatialautocorrelation(SA)inmyvariables(abundanceandrichnessofbird andtreespecies).IevaluatedSAusingtheMoran’scoefficientincorrelograms (I=between0.55to0.85fortreesand0.22to0.19forbirds).Moran coefficient(I)describesthedegreeofcorrelationbetweenthevaluesofa variableasafunctionofspatiallocations(Fortin1999).Moran’sIindicates positiveautocorrelationwithpositivevalues(usually0to1),negative autocorrelationwithnegativevalues(0to1),andtheabsenceof autocorrelationiscloseto0(Legendre1993;Rosenberg2001).Becausethe individualcoefficientsofthecorrelogramarenotindependentfromone anotherIdeemedthecorrelogramassignificantifthesignificancelevelofat leastoneindividualcoefficientwaslowerthantheα´level(α´=0.004),using theBonferroniadjustment(Fortin1999).Imade12distanceclasses.Because SAIusedaconservativemeasurelevelofsignificance(α=0.01)intheanalysis (Guénette&Villard2005).AdjustingtheαleveldoesnotcorrectSApersebut doesprovidesomeassurancethatsignificantresultsdetectedareindeed significant(Dale&Fortin2002).However,marginallysignificantvalues(α= 0.02)wereconsideredforlogisticregressionmodelsandthresholdcalculations, ROCcurves(seebelow). Toestablishifrichnessandabundanceoffrugivorousbirdswererelatedto richnessandabundanceofkeyfruitingtreeswithineachlandscapeandamong landscapes,IusedaManteltest(Fortin1999;Fortin&Dale2005).Thistest wasselectedbecausemybirdandfruitingtreesdatawerecollectedinthesame sites,andtheobjectiveoftheMantelTestistolookforcorrelationbetween spatiallyautocorrelateddata(Fortin&Dale2005).Ibuiltthedistancematrices ofspeciesrichnessandabundanceusingEuclideandistance.Forsignificance evaluationIusedMonteCarlotestrandomizations(5000).Ievaluatedthe relationshipbetweenpatchareaandtotalabundanceoffruitingtreespecies (Cecropia, Ficus and Miconia )usingSpearmanCorrelation. Irelatedthefrugivorousbirdspeciesabundancewiththeselectedexplanatory variables(Table2)atthreedifferentecologicalscales(local,3ha;intermediate, 312haandlandscape,2500ha)usingCanonicalCorrespondenceAnalysis (CCA).Theaimofcanonicalordinationistodetectthemainpatterninthe relationsbetweenthespeciesandtheexplanatoryenvironmentorhabitat variables(terBraak1986,1987).Iassessedindividualvariablesinthefinal

CBMMasterThesesNo.41 13 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

modelbycalculatingtheintrasetcorrelations.Thisgavemethecorrelation betweenalandscapevariableandanaxis,whichisameasureoftherelative importanceofthatparticularvariabletotheaxis.Thegraphicaloutput resultingfromanordinationisabiplot.Vectorinthebiplotrepresentsthe correlationbetweenanexplanatoryvariableandtheCCAaxes(terBraak1986; Coppedgeetal.2001).ThesignificancewasevaluatedbyconductingMonte Carlorandomizationsonthefrugivorousbird–explanatoryvariables relationship.AsIhaddifferentsamplingeffortamongquadrantsand landscapes,Iusedmeanabundanceoffrugivorousbirdspeciesandkeyfruiting trees.Toestablishthekeyfruitingtreerichnessineachquadrantand landscape,Iusedrarefactionindividual–based(forintermediatescaleI compareamongquadrantsusingn=20individuals;andforlandscapescale usingn=150indiv.)(Gotelli&Colwell2001). Table2:Explanatoryvariablesselectedtoevaluatetherelationshipbetweenlandscape characteristicsandkeyresourcedistributionintheCentralAndesofColombia.*To avoidpseudoreplicationeffects,PatchAreavariablewasonlyconsideredforlogistic regressionanalysisbecauseinsomecaseswehadabigpatch(>200ha)withmore thanonesamplingpoints.Thenallsamplingsinonebigfragmentweresummarizedin onesampleusingpresence–absencedataofthespeciesandonlyoneareavalue. EcologicalScale Abbreviation Variable Local(3ha) Patch_Area* Patcharea Num_LC Numbersoflandcoverswithinthe100m bufferring HA100 Suitableamountofhabitat(Forest)within the100mbufferring EL100 Forestedgelengthwithinthe100mbuffer ring Treerich Keyfruitingtreestotalrichness Treeabun Keyfruitingtreestotalabundance Abu_Ficu Abundanceof Ficus Abu_Cecr Abundanceof Cecropia Abu_Mico Abundanceof Miconia Intermediate(312ha) Suit_Am_Habit Suitableamountofhabitat(Forest) and Landscape(2500ha) Num_LC Numbersoflandcovers Num_Patch Numberofforestpatches EL Forestedgelength Treerich Keyfruitingtreerichness(n=20and150 indiv.) Treeabun Keyfruitingtrees(meanabundance) Abu_Ficu Meanabundanceof Ficus Abu_Cecr Meanabundanceof Cecropia Abu_Mico Meanabundanceof Miconia Selectionofspeciesforthresholdanalyseswasmadeusingtwocriterions:First, speciesonlypresenton≥10%or≤90%ofthe76sites,wereincluded because,thresholdeffectscannotbederivedforveryrareorverycommon (Trzcinskietal.1999;Gutzwiller&Barrow2001).Second,speciesnegatively

CBMMasterThesesNo.41 14 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

affectedbyhabitattransformation(Mönkkönen&Reunanen1999;Guénette &Villard2004).Incaseofpresence/absencedatafocusingonfocalspeciesis recommendedformanagementpurposes(Mönkkönen&Reunanen1999), becauseforinstanceinthecaseofnegativelyaffectedbyhabitat transformationspeciestheirmajorhabitatrequirementscouldencapsulate thoseoflesssensitivespeciesfoundinthesameguild.Thesenegatively affectedspecieswereidentifiedthroughadetrendedcorrespondenceanalysis (DCA)usingascatterdiagram(terBraak1987)(Fig.3)andtheCCAresults. Speciesrelatedtothelandscapeswithhigheramountofforestcoverandwhich werenotpresentinhighlyfragmentedlandscapeswereconsideredas negativelyaffectedbyhabitattransformation.Thirtytwothreespeciesmet bothcriterions(Table1). DCA fbirds abund Tlabr

Pchal Aabur Cniti Pauri Prief Ccyan Cgoud Hfron Bmont Tserr Salbo Pscut NBS7

Ccani Pleuc M rall 2 OBM 8 1 Ppiti OBM 3 OBM 1 Apras Ppers FB3 OBS4 OBS7 M oliv NBM 6 NF72 NBM 81 OBM 6 NC6 Pmela M ychry OBM 2 Txant NF71 NBM 82 Aflav Ahaem OBM 72 NF8 NC8 Emusi OBS5 Ptumu NC11 NBS11 OBM 5 FF4 OBM 71 M chry NC4 NBS8 OBS2 NC2 FB8 FF52 FB7 OBS8 Exant NF73 NBS3 FB6 OBS3 NBS12 FB4 FB5 Copht FB1 OBS6 Hsupe NF4 Zviri NBS41 FC8 FC4 FB2 Dcyan Awagl CHFBR6 CHFBD42 NC12 NBS42 FF8 FF6 OBS1 4 NBS2 FF51 Axis 2 Axis NC3 NC5 CHFBD1 FC1 CHFBD3 CHC4 CHC1 Plleucs CHFBD41 M stri Omomo CHFBR5FC7 Dalbi CHFBD8 Hcris FC2 Tvitr Salbic CHFBR7 FC6 Tfusc CHC8 FC5 Ebour CHC5 Satri Tvasso Tarth CHC6 CHC7 Thein Tnigr CHC3 CHC2 Amerc Tigno 3 Cfasc Tgyro Tepis Hguir Tpalm Rflam

Cspiz

Tcyan Fig.3:GroupingofsamplingsitesaccordingwithtAxis 1 heirfrugivorousbirdspecies compositionintheCentralAndesofColombiausingDCA.Crossesarebirdspecies.Full birdnamesareinTable1.Trianglesaresites(startingwithCHarefromChambery;F fromFilandia;OfromOtúnandNfromNima).Solidlinecirclesnumber1,2and3 correspondtoOtún,NimaandChamberyrespectively,dashedlinecirclenumberfour groupingtheFilandia’ssites.

CBMMasterThesesNo.41 15 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Iusedstepwise(forward)logisticregressionstoevaluaterelationshipsbetween thepresenceandabsence(P/A)ofsinglespecieswiththeexplanatoryvariables (landscapeandkeyfruitingresourcevariables).Thisapproachisbasedonthe probabilityofWaldstatistic(p<0.001forenterandp>0.10forremoval (Guénette&Villard2005).Iranthelogisticregressionsforlocalscale, intermediateandlandscapescales.Toestablishspeciesspecificecological thresholdsIusedsinglespecificexplanatoryvariables(Table2).Itransformed thedatausinglogarithmictransformations(Zar1984). Toassesstheperformanceoftheregressionmodelsandidentifythethreshold values,Iusedthresholdindependentreceiveroperationcharacteristic(ROC) curves(Guénette&Villard2004,2005).EachpointontheROCplot representsasensitivity/specificitypaircorrespondingtoaparticulardecision threshold.Atestwithperfectdiscrimination(nooverlapinthetwo distributionsofresults)hasaperfectsensibility(1.0)andperfectspecificity (0.0)(Zweig&Campbell1993).Areaundercurvevalues(AUC)with significanceshigherthan0.02werearbitrarilyconsiderednondifferentof0.5 (0.5AUCvaluescorrespondstothetheoreticalplotforatestwithno discriminationbetweenthetwodistributionsofresults).Toidentifythe optimumprobabilitythresholdIusedthemaximumaccuracymethod,the pointatwhichthesumofsensitivityandspecificityismaximized(Maneletal. 2001;Guénette&Villard2005).TheROCcurvesmethodappearsasoneof thebestmethodstoestablishecologicalthresholdscomparedwithothers approaches(Maneletal.2001;Liuetal.2005).Usually,AUCvaluesof0.5– 0.7aretakentoindicatelowaccuracy,valuesof0.7–0.9indicateuseful applicationsandvaluesof>0.9indicatehighaccuracy(Maneletal.2001).I evaluatedthemodelfittoeachscalecomparingtheareaundercurve(AUC) andNagelkerke’sR 2,thoughSpearmancorrelation(Gutzwiller&Barrow2001; Guénette&Villard2005).IranthistestusingSigmaPlot10. Tovalidatethethresholdvaluesthesiteswhereeachspeciesispresentand whereisabsent,accordingwiththevalueobtainedfortheexplanatoryvariable, wererecorded.Forvariableswhichhaveanegativerelationshipwithforestand forest–edgespecies,belowthethresholdthepresenceofthespeciesis expected.Forvariableswithpositiverelationshipwiththespeciesabovethe thresholdthepresenceisexpected.However,inallcasessomefalsenegatives (absenceofthespeciesinsiteswheretheirpresencewasexpected)andsome falsepositives(presenceinsiteswheretheirabsencewasexpected)occurred, butinlessproportionofthetruepositivesandnegatives(Zweig&Campbell 1993).

CBMMasterThesesNo.41 16 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Results

Relationship between abundance and richness of birds and resources Amonglandscapestherichnessandabundancedistributionoffrugivorous birdswerepositivelycorrelatedwiththerichnessandabundanceoffruiting treesofgenera Ficus, Cecropia and Miconia (Manteltest;r=0.184and0.119 respectively;p≤0.001).Withineachlandscapeseparatelythecorrelationswere notsignificant,eventhoughforNimaandOtunlandscapeswhichsignificance valuescouldmotivatefurtherresearchtoexploretheserelationships(Table3). Table3:Manteltestresultsforeachoneoftherelationshipsevaluatedbetween frugivorousbirdspeciesabundance/richnessandkeyfruitingtrees( Ficus, Cecropia and Miconia )abundance/richnessonlocalscaleintheCentralAndesofColombia. Landscape Relationshipevaluated StandardMantel pvalue Statistic(r) Alllandscapes Frut.treesrichnessvs.Frug.birdsrichness 0.184 0.0002 n=76 Frut.treesabundancevs.Frug.birdsabundance 0.119 0.0006 Chambery Frut.treesrichnessvs.Frug.birdsrichness 0.09 0.17 n=16 Frut.treesabundancevs.Frug.birdsabundance 0.10 0.26 Filandia Frut.treesrichnessvs.Frug.birdsrichness 0.07 0.31 n=20 Frut.treesabundancevs.Frug.birdsabundance 0.16 0.18 Nima Frut.treesrichnessvs.Frug.birdsrichness 0.20 0.03 n=24 Frut.treesabundancevs.Frug.birdsabundance 0.08 0.21 Otún Frut.treesrichnessvs.Frug.birdsrichness 0.24 0.04 n=16 Frut.treesabundancevs.Frug.birdsabundance 0.22 0.13 Birds – explanatory variables relationship Atlocalscale(3.14ha)andforabundancedataoffrugivorousbirdspeciesthe threefirstCCAaxesaccountedfor42.8%ofthetotalvarianceinthespecies data(axis1:24.9%;axis2:17.8%andaxis3:0.1%),and84%oftheextracted varianceinthespecies–explanatoryvariablesrelationship.TheMonteCarlo testofrelationshipsshowedthatboththefirstCCAaxis(p<0.01)andthe overallanalysis(p<0.01)weresignificant.Axis1isbetterexplainedbythe LandscapeCharacteristics,suitablehabitatamountwithinthe100mbufferring (HA100);numbersoflandcoverwithinthe100mring(Num_LC)andedge lengthwithinthe100mbufferring(EL100).Thefirstonehadoppositesignto theothertwo(Table4).Axis2isbetterexplainedbyFruitResources Distribution,thismeansthevariablesrelatedwithkeyresourcesoffer( Ficus, Cecropia and Miconia ).Abundanceof Cecropia (Abu_Cecr)hadoppositebehavior totheothervariables:keyfruitingtreestotalspeciesrichness(Treerich);key fruitingtreestotalabundance(Treeabun);Abundanceof Ficus (Abu_Ficu)and Abundanceof Miconia (Abu_Mico)(Table4).

CBMMasterThesesNo.41 17 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

ThemajorityoftheOtún’ssitesandsomecharacteristicforestspecies(i.e. , Aratinga wagleri, Hemispingus frontalis, Penelope perspicax, Pharomachrus auriceps, Pionus tumultuosus, Pyroderus scutatus, Sericossypha albocristata, Masius chrysopterus, Pipreola riefferii )arepositivelycorrelatedwithHA100andnegativelycorrelated withNum_LCandEL100. Tangara vitriolina and Turdus serranus arepositively correlatedwithNum_LCandEL100.TherestofOtúnandtheFilandia’ssites arepositivelycorrelatednotonlywithHA100butalsowithTreerichand Treeabun.Speciessuchas Aburria aburri, Chlorochrysa nitidissima, Aulacorhynchus prasinus, Chlorospingus ophthalmicus, Mionectes olivaceus, Piranga leucoptera, Anisognathus flavinucha, Euphonia xanthogaster, Habia cristata havethesame behavior(Fig.4). TheChambery’ssitesandspeciessuchas Columba fasciata, Saltator atripennis, Tangara heinei, Tangara vitriolina, Turdus fuscater, Turdus ignobilis arepositively correlatedwithTreerich;Treeabun;Abu_FicuandAbu_Mico.Themajorityof Nima’ssitesandspecieslikea Buthraupis Montana, Chlorospingus canigularis, Hemispingus superciliaris, Ortalis motmot, Saltator albicollis arenegativelycorrelated withthesevariablesandarepositivelycorrelatedwithAbu_Cecr.Inbothcases, thedistributionofthesespeciesandsitesofChamberyandNimaare influencedbyNum_LCandEL100(Fig.4). Atintermediatescale(312.5ha)andforabundancedataoffrugivorousbird speciesthethreefirstaxesaccountedfor59%ofthevarianceinthespecies data(axis128.3%;axis218.4%andaxis312.2%)and97%oftheextracted varianceinthespecies–explanatoryvariablesrelationship.TheMonteCarlo testofrelationshipsshowedthatboththefirstCCAaxis(p<0.01)andthe overallanalysis(p<0.01)weresignificant.Axis1wasbetterexplainedagainby LandscapeCharacteristics,especiallybySuit_Am_Habit(nativeforest)and Num_LC.However,Suit_Am_Habithadacontrarybehaviorrespect Num_LC,ELandNum_Patch(Table13andFig.5).Axiss2and3were explainedbyFruitResourcesAvailability.FortheAxis2,Treerichand Abu_FicuhadoppositebehaviortotheothervariablesTreeabun,Abu_Cecr andAbu_Mico(Table5). Otun’squadrantsandsometypicalforestspecies(i.e. Aburria aburri, Penelope perspicax, Piranga leucoptera, Pyroderus scutatus )aremainlycorrelatedwith Suit_Am_Habit.Thedistributionof Chlorochrysa nitidissima and Pipreola riefferii arepositivelycorrelatedwithSuit_Am_Habit,butNum_Patchinfluencedon thefinallocationinthebiplot.TheFilandia’squadrantsarealsopositively

CBMMasterThesesNo.41 18 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

6 Abu_Ficu Treeabun

Tcyan 4.8 Abu_Mico Dalbi TpalmCspiz treerich

3.6 Rflam Hguir

Tepis 2.4 EL100 Ccyan CfascTgyro CHC2TfuscMstri Tvasso CHC7CHFBR7 1.2 TignoCHC6 Txant Num_LC CHC3 Tnigr CHC5Ebour CHC8FC5TheinFC2 Aabur CHFBD8SatriFC1FC7CHC1OBS1Tarth Tvitr CHFBD1FC6FC4CHFBD3FF8CHFBR5OBS6 Hcris Cniti TlabrCHC4CHFBD42AmercAprasCopht 0 FC8FF51FF6Emusi Pleuc Fruit Resources Distribution Resources Fruit CHFBR6Aflav Moliv Tserr CHFBD41PmelaFF52OBS3OBS5OBS4OBS2Exant NBS7PchalZviriFB1FB2OBS8OBM6OBM3OBS7FB5OBM71OBM72Mchry NC3NC5NBS41NBS42NC8NBS8OBM5FB7FB3OBM1FF4OBM2FB6Ppers NBS12NF4NF8NC2NF73NBM81FB8FB4NBM82OBM8 Hfron NBM6NBS3NC11NC6NBS11NF72AhaemCgoudMychry PscutAwaglPrief SalbicNBS2NC12NF71NC4Mrall OmomoPpiti PtumuPauri -1.2 Ccani Salbo Hsupe Bmont Plleucs

-2.4 Abu_Cecr Dcyan HA100 -3.6 -10 -7.5 -5 -2.5 0 2.5 5 7.5 Landscape Characteristics Fig.4:OrdinationbiplotdepictingthefirsttwoaxesoftheCCAof76sites(localscale) with58frugivorousbirdspeciesoftheCentralAndesofColombia.9vector representingequalnumberofvariables.Labelswithdotarebirdspecies.Fullbird namesareinTable2.Site’slabels(incapitalletters)startswithCHarefromChambery; FfromFilandia;OfromOtúnandNfromNima. Table4:Intrasetcorrelationsbetweenlandscape/resourcevariablesandCCAaxes1, 2and3atlocalscaleforthefourstudiedlandscapesintheCentralAndesofColombia. CompletenameofthevariablesareinTable2. Abbreviation Axis1 Axis2 Axis3 Num_LC 0.911 0.051 0.105 HA100 0.723 0.303 0.413 EL100 0.683 0.284 0.291 Treerich 0.230 0.452 0.391 Treeabun 0.153 0.639 0.396 Abu_Ficu 0.128 0.609 0.378 Abu_Cecr 0.162 0.265 0.757 Abu_Mico 0.069 0.543 0.057 correlatedwithSuit_Am_HabitandAbu_Mico,buttheirdistributionishighly influencedbyNum_PatchandELandinlowerlevelbyTreerichand Abu_Ficu(Fig.5).Speciessuchas Diglossopis cyanea, Mionectes striaticollis, Myadestes ralloides, Saltator atripennis, Thraupis episcopus, Turdus ignobilis arepresentin Filandiaandalmostallarecharacteristicofedgeandopenareas(Fig.5).

CBMMasterThesesNo.41 19 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

ThequadrantsofNimaandChambeyarenegativelycorrelatedwith Suit_Am_Habitandarecharacterizedbyspeciesfromedgeandopenareas(i.e. Hemithraupis guira, Ortalis motmot, Tangara vitriolina ).Mainly,theChambery’s quadrantsarepositivelycorrelatedwithEL,Num_Patch,Num_LCand Treeabund,andnegativelycorrelatedwithTreerichandAbu_Ficu.Specieslike Tangara gyrola, Chlorophanes spiza, Tangara heinei, Tangara xanthocephala are positivelycorrelatedwithEL,Num_PatchandTreeabun(Fig.5).Themajority ofNima’squadrantsarepositivelycorrelatedwithTreerich,Abu_Ficuand Abu_Cecr.Forestspecieslikea Amazona mercenaria, Aulacorhynchus haematopygus, Chlorospingus canigularis, Chlorospingus ophthalmicus and Hemispingus superciliaris are alsopositivecorrelatedwithTreerich,Abu_FicuandAbu_Cecr(Fig.5). Pchal TserrBmont 3 treerich Abu_Ficu N7 2 Tlabr Ccani 1 Hsupe Copht Amerc Ccyan AhaemN6 Hfron Cgoud PpitiPmelaEmusi F3HcrisO5O1N8 Abu_CecrSalbicRflam 0 Pleuc PpersPauriO3O7AprasMychryO6AflavMrallN1N2N3 CfascTcyanHguir Suit_Am_Habit Aabur TnigrF5 N4CH8Tvitr PscutO8O2 F8TheinCH7N5 Omomo Ptumu O4 Abu_MicoF1 CH5CH3CH4CH2 ExantF6F4ZviriEbourCH1TxantTgyro Salbo Moliv F7TarthCH6 Satri Treeabun -1 MchryPlleucsF2 Tvasso Awagl

Resources Distribution Fruit Mstri DalbiDcyan TepisTfuscCspiz Tigno Cniti Tpalm Prief Num_LC -2 -3

EL -4 Num_Patch -12 -9 -6 -3 0 3 6 9 Landscape Characteristics Fig.5:OrdinationbiplotdepictingthefirsttwoaxesoftheCCAof32quadrants(312 ha)with58frugivorousbirdspeciesoftheCentralAndesofColombia.9vector representingequalnumberofvariables.Labelswithdotarebirdspecies.Fullbird namesareinTable2.Site’slabels(incapitalletters)startswithCHarefromChambery; FfromFilandia;OfromOtúnandNfromNima. Atlandscapescale(2500ha)IdidnotfindsignificantresultsaftertheMonte CarlotestmainlybecauseIhadnotenoughreplicates.

CBMMasterThesesNo.41 20 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Table5:Intrasetcorrelationsbetweenlandscape/resourcevariablesandCCAaxes1, 2and3,atintermediatescale,forthefourstudiedlandscapesintheCentralAndesof Colombia.CompletenameofthevariablesareinTable2. Abbreviation Axis1 Axis2 Axis3 Suit_Am_Habit 0.881 0.055 0.141 Num_LC 0.839 0.240 0.330 Num_Patch 0.341 0.394 0.385 EL 0.371 0.325 0.657 Treerich 0.131 0.398 0.148 Treeabun 0.265 0.049 0.197 Abu_Ficu 0.218 0.215 0.577 Abu_Cecr 0.110 0.037 0.200 Abu_Mico 0.083 0.011 0.003

Atlocalscale,14speciesshowedsignificantrelationshipswiththeexplanatory variables.Tenoutthefourteenforestspeciesselectedasnegativelyaffectedby habitattransformationhadahighlysignificantrelationshipswithoneormore explanatoryvariables.Fortheforest–edgespecies,onlyfourspeciesshowed highlysignificantrelationships(Table6).Patcharea,numberoflandcover (Num_LC)andedgelength(EL100)werethevariableswhichmostofthe selectedspeciesshowedstrongrelationships.InalmostallcasesNum_LCand EL100hadnegativerelationshipswiththepresenceofthespecies.Onlytwo species( Euphonia musica and Hemispingus superciliaris )hadsignificant relationshipswithfruitresources(Table6). Table6:Resultsofthestepwiselogisticregressionmodelsofthespeciespresence relatedtoexplanatoryvariablesatlocalscale(n=76).Probability,**p≤0.01; ***p≤0.001.Marginallysignificantvaluesareshowninbrackets(p≤0.02).10forest speciesinboldand4forest–edgespecies.Completenameofthefrugivorousbird speciesandexplanatoryvariablesareinTables1and2respectively. AbbreviationAbbreviationSinglespecific βββ1111 variablevariable AhaemAhaem HA100 5.943** AprasApras Num_LC 7.806** Patch_Area 1.277** ExantExant Patch_Area 1.515** Num_LC 13.177*** EL100 0.972*** HsupeHsupe Treerich 5.850** Treeabun 3.293** Num_LC 7.782(0.014) MychryMychry Patch_Area 1.829** HA100 9.180** MolivMoliv Patch_Area 2.371** EL100 0.773(0.014) MrallMrall HA100 5.970(0.011) EL100 3.109(0.019) PpersPpers Patch_Area 3.388*** Num_LC 11.811*** EL100 1.028***

CBMMasterThesesNo.41 21 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

HA100 36.944(0.014) PauriPauri Num_LC 12.229** EL100 1.052** Patch_Area 1.584(0.019) PscutPscut Patch_Area 4.369*** Num_LC 15.054*** EL100 1.323*** HA100 65.776(0.016) Aflav Patch_Area 2.367*** HA100 7.982(0.011) Awagl Patch_Area 2.047** EL100 0.649(0.014) Emusi Abu_Mico 5.084** Pchal Patch_Area 2.308*** Num_LC 7.586** EL100 0.833** HA100 16.297(0.02) Atintermediatescale,sevenspecieshadasignificantrelationshipwiththe explanatoryvariables.Fiveofthesespeciesshowedapositiverelationshipwith forestcovervariable(Suit_Am_Habit)(Table7). Euphonia xanthogaster which showedpositiverelationshipwiththeforestcovervariablewasnegatively correlatedtolandscapeconfigurationvariables–Num_LC(Table7).Similarly tolocalscale,onlyonespeciesshowedsignificantrelationshipwithfruit resources( Aulacorhynchus haematopygus ).Fiveoutofthe14specieswhichhada significantresponseatlocalscale,showedacongruentresponseatintermediate scale,thismeansrespondedsignificantlytoforestcovervariables. A. haematopygus showedresponsetoadifferentvariableatlocalandintermediate scales,andonlyonespeciesshowedresponseonlyatintermediatescale (Tangara gyrola )(Table7).Forlandscapescale,nosignificantrelationshipswere found. Thecorrelationbetweenpatchareaandtotalabundanceoffruitingtreespecies Ficus, Cecropia and Miconia ,waspositiveandsignificant(SpearmanCorrelation;r =0.375;p=0.003).Thismeansthatincreasingpatchareamorepresenceof individualsofthosekeyfruitresourcesareexpected.

CBMMasterThesesNo.41 22 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Table7:Resultsofthestepwiselogisticregressionmodelsofthespeciespresence relatedtoexplanatoryvariablesatlocalscale(n=32)atintermediatescale. Probability,**p≤0.01;***p≤0.001.Marginallysignificantvaluesareshownin brackets(p≤0.02).Fiveforestspeciesinboldand2forest–edgespecies.Complete nameofthefrugivorousbirdspeciesandexplanatoryvariablesareinTables1and2 respectively. AbbreviationAbbreviationSinglespecific βββ1111 variablevariable AhaemAhaem Abu_Ficu 6.929(0.015) ExantExant Suit_Am_Habit 9.594** Num_LC 24.045*** MolivMoliv Suit_Am_Habit 5.179(0.014) PpersPpers Suit_Am_Habit 6.373** PscutPscut Suit_Am_Habit 5.781** Pchal Suit_Am_Habit 4.808(0.018) Tgyro Num_LC 11.294** Ecological Thresholds AftertheROCanalysis,andtodeterminethresholdsinspeciesresponseat localscaletotheexplanatoryvariables(Table2),onlysignificantAUCvalues wereused.Thisprocedurediscardseightrelationshipsforfurtheranalysis.No relationshipswerediscardedatintermediatescale. TheAUCvaluesforallspecies(14)atlocalscalewerepositivelyandhighly significantcorrelatedwithNagelkerke’sR 2(SpearmanCorrelation;r=0.82,p <0.001).Thus,AUCandR 2providesimilarassessmentofmodelfit(Guénette &Villard2005).Atintermediatescale,therelationshipwasnotsignificant becausethereweretoofewpointsforthecorrelationanalysis. Atlocalscalethespecieswhichexhibitingthehighestdiscriminationbetween presenceandabsencebasedonforestcovervariables(Patch_AreaandHA100) were Mionectes olivaceus (AUC=0.865), Penelope perspicax (AUC=0.898)and Pyroderus scutatus (AUC=0.927)forPatch_Area(Fig.6)and Penelope perspicax (AUC=0.859)and Pyroderus scutatus (AUC=0.902)forHA100.Ontheother hand,basedonlandscapeconfigurationvariables(Num_LC;EL100)the highestvalueswereagain Penelope perspicax (AUC=0.841), Pyroderus scutatus (AUC=0.901), Pharomachrus auriceps (AUC=0.863)(Fig.6)and Pyroderus scutatus (AUC=0.852), Pharomachrus auriceps (AUC=0.815), Penelope perspicax (AUC=0.805)respectively(Table8).Atintermediatescalethespecies exhibitingthehighestdiscriminationbetweenpresenceandabsencebasedon Suit_Am_Habitwere Euphonia xanthogaster (AUC=0.91), Penelope perspicax (AUC=0.854) , Pyroderus scutatus (AUC=0.85)(Table9;Fig.7). Ingeneral,thethresholdvaluesvalidationshowedthatatlocaland intermediatescalesthenumberoftruepositiveswashigherthanthenumberof falsepositives(Tables10and11).Inonlyonecasethenumberoftrue

CBMMasterThesesNo.41 23 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

positiveswaslowerthanthenumberoffalsepositives( Aulacorhynchus haematopygus )(Table10).Thiscouldbeexplainedbecausetheloweraccuracyin thethresholdidentificationbytheAUCvalue(0.69,Table8). Table8:Thresholdvalues(cutoffvaluec,establishedwithmaximumaccuracy)atlocal scaleintheoccurrenceof14species(10forestspeciesinboldand4forest–edge species)withstrongrelationshipwithsinglelandscapeandkeyresourcesexplanatory variables.Thesignofrelationshipwasestablishedbasedonlogisticregressionresults, Table6.Probability,**p≤0.01;***p≤0.001.Marginallysignificantvaluesareshownin brackets.Completenameofthefrugivorousbirdspeciesandexplanatoryvariablesare inTables1and2respectively. Single Abbreviation AUCAUCThreshold UnitsUnitsSignof specific valuvalue(c)e(c)e(c) relationship variablevariable between speciesand variablesvariables HA100AhaemAhaem 0.695** 2.99 Hectares(ha) + MychryMychry 0.728*** 2.77 ha + MrallMrall 0.742** 2.10 ha + PpersPpers 0.859*** 2.79 ha + PscutPscut 0.902*** 2.88 ha + Aflav 0.673(0.017) 2.16 ha + Pchal 0.803*** 2.79 ha + Num_LCAprasApras 0.722*** 1.5 Landcovers ExantExant 0.801*** 2.5 Landcovers PpersPpers 0.805*** 1.5 Landcovers PauriPauri 0.815** 1.5 Landcovers PscutPscut 0.852*** 1.5 Landcovers Patch_AreaMychryMychry 0.753*** 7.88 ha + MolivMoliv 0.865** 97.83 ha + PpersPpers 0.898*** 97.83 ha + PscutPscut 0.927*** 57.28 ha + Aflav 0.83*** 7.88 ha + Awagl 0.79** 97.83 ha + Pchal 0.769(0.015) 57.28 ha + EL100ExantExant 0.714** 187.25 Meters(m) PpersPpers 0.841*** 180.68 m PauriPauri 0.863*** 127.55 m PscutPscut 0.901*** 127.55 m MrallMrall 0.803*** 452.99 m Pchal 0.813*** 127.55 m Awagl 0.753** 399.12 m TreerichHsupeHsupe 0.728** 2.5 Species

CBMMasterThesesNo.41 24 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Penelope perspicax Pyroderus scutatus

1 1

0.5 0.5 Probability of Presence Probability of presence

0 0 0 50 100 150 200 250 300 350 400 450 500 550 0 50 100 150 200 250 300 350 400 450 500 550 Patch Area (ha) Patch Area (ha)

Mionectes olivaceus Penelope perspicax

1 1

0.5 0.5 Probability of Presence Probability of Presence

0 0 0 50 100 150 200 250 300 350 400 450 500 550 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 Patch Area (ha) Number of Land-covers

Pharomachrus auriceps Euphonia xanthogaster

1 1

0.5 0.5 Probability of Presence Probability of Presence

0 0 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 Number of Land-covers Number of Land-covers Fig.6:Probabilityofpresenceofspecieswhichexhibitingthehighestdiscrimination betweenpresenceandabsencebasedonforestcovervariable(Patch_Area)and landscapeconfiguration(Num_LC)atlocalscale.Dashedlinesrepresent95% confidenceintervals.VerticaldashedlineindicatesthresholdsdeterminedusingROC analysis.Curvesweresmoothedusingalocalsmoothingtechniquewithtricube weightingandpolynomialregression.

CBMMasterThesesNo.41 25 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Table9:Thresholdvalues(cutoffvaluec,establishedwithmaximumaccuracy)at intermediatescaleintheoccurrenceof8species(6forestspeciesinboldand2forest –edgespecies)withstrongrelationshipwithsinglelandscapeandkeyresources explanatoryvariables.Thesignofrelationshipwasestablishedbasedonlogistic regressionresults,Table7.Probability,**p≤0.01;***p≤0.001.Completenameofthe frugivorousbirdspeciesandexplanatoryvariablesareinTables1and2respectively. Singlespecific AbbreviationAbbreviationAUCAUC Threshold UnitsUnitsSignofrelationship variablevariable value(c)value(c) betweenspecies andvariablesandvariables ExantExant Hectares Suit_am_habit 0.91*** 83.74 (ha) + PpersPpers 0.854** 121.74 ha + PscutPscut 0.85** 206.62 ha + MolivMoliv 0.802(0.012) 121.74 ha + Pchal 0.818** 83.74 ha + Num_LCExantExant 0.804** 3.5 Landcovers Tgyro 0.794** 4.5 Landcovers + Abu_FicuAhaemAhaem 0.843** 2.25 Individuals + Penelope perspicax Euphonia xanthogaster

1 1

0.5 0.5 Probability ofof PresencePresence Probability ofof PresencePresence

0 0 0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 Suitable Amount of Habitat (ha) Suitable Amount of Habitat (ha) Pyroderus scutatus

1

0.5

Probability of Presence

0 0 20 40 60 80 100 120 140 160 180 200 220 240 260 280 Suitable amount of Habitat (ha) Fig.7:Probabilityofpresenceofspecieswhichexhibitingthehighestdiscrimination betweenpresenceandabsencebasedonforestcovervariable(Suit_Am_Habit)at intermediatescale.Dashedlinesrepresent95%confidenceintervals.Verticaldashed lineindicatesthresholdsdeterminedusingROCanalysis.Curvesweresmoothedusing alocalsmoothingtechniquewithtricubeweightingandpolynomialregression.

CBMMasterThesesNo.41 26 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Table10:Thresholdvalidationatlocalscalebasedonthenumberoftruepositivesand truenegativesversusthefalsepositivesandfalsenegatives.Completenameofthe frugivorousbirdspeciesandexplanatoryvariablesareinTables1and2respectively. Singlespecific AbbreviationAbbreviationThreshold True False variablevariable value(c)value(c) PositivesPositives PositivesPositives HA100AhaemAhaem 2.99 17 23 MychryMychry 2.77 21 11 MrallMrall 2.10 44 16 PpersPpers 2.79 12 1 PscutPscut 2.88 12 0 Aflav 2.16 20 3 Pchal 2.79 12 1 Num_LCAprasApras 2.5 25 2 ExantExant 2.5 27 1 PpersPpers 1.5 7 6 PauriPauri 1.5 5 3 PscutPscut 1.5 8 4 Patch_AreaMychryMychry 7.88 20 4 MolivMoliv 97.83 5 2 PpersPpers 97.83 8 2 PscutPscut 57.28 9 1 Aflav 7.88 18 3 Awagl 97.83 5 3 Pchal 57.28 6 2 EL100ExantExant 187.25 20 8 PpersPpers 180.68 12 1 PauriPauri 127.55 7 1 PscutPscut 127.55 11 1 MrallMrall 452.99 44 16 Pchal 127.55 10 3 Awagl 399.12 12 1 TreerichHsupeHsupe 2.5 9 8 Table11:Thresholdvalidationatintermediatescalebasedonthenumberoftrue positivesandtruenegativesversusthefalsepositivesandfalsenegatives.Complete nameofthefrugivorousbirdspeciesandexplanatoryvariablesareinTables1and2 respectively. Singlespecific AbbreviationAbbreviationThreshold True False variablevariable value(c)value(c) PositivesPositives PositivesPositives Suit_am_habit ExantExant 83.74 16 1 PpersPpers 121.74 7 1 PscutPscut 206.62 6 3 MolivMoliv 121.74 7 1 Pchal 83.74 8 0 Num_LC ExantExant 3.5 16 1 Tgyro 4.5 10 2 Abu_Ficu AAAhaemAhaemhaem 2.25 19 3

CBMMasterThesesNo.41 27 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

Discussion Ingeneralmyresultsindicatethat,thedistributionoffrugivorousbirdspecies intheCentralAndesofColombiaisbetterexplainedatlocalandintermediate scalesbylandscapecharacteristics,especiallyforestcover,thanfruitresources distribution.Atlocalscale(3ha)Iestablished27speciesspecificoccurrence thresholdsforfourlandscapecharacteristicvariables(forestcoverand landscapeconfiguration)andonefruitresourcesvariable,for14forest frugivorousbirdspecies.While,atintermediatescale(312ha)Iseteight occurrencethresholdsintwolandscapecharacteristicvariablesandonefruit resourcedistributionvariableforsevenbirdspecies. MyresultsaboutthresholdsvaluesarenovelforNeotropicallandscapesand thisisoneofthefirstempiricalstudiesconductedatdifferentscales.Other studiespresentingempiricalthresholdvaluescomemainlyfromtemperateand subtropicalregions,andaremostoftenrelatedwithchangesinhabitat amount.Severaltaxahavebeeninvestigated,e.g.birds(Vanceetal.2003; Bennet&Radford2004;Radfordetal.2005;Guénete&Villard2005;Suorsa etal.2005),lizards(Lindenmayeretal.2005);frogs,fungi,plants(Drinnan 2005;Bascompte&Rodriguez2001),squirrels(Rodriguez&Andrén1999) andbutterflies(Schultz&Crone2005). RecentlyGuénette&Villard(2004,2005)setspeciesspecificecological thresholdsusingROCcurves.Theyarguedthatusingsinglevariablesrarely succeedsincapturingcomplexchanges.Insteadtheyusedsyntheticvariables (multivariateaxesinaPrincipalComponentAnalysis)tosettheirthreshold values.Furthermore,theyproposedthatthismethodcouldbeusefulto examinethresholdsinbirdresponsetospecifichabitatvariables.Myresults supportempiricallythislastaffirmationandIconsiderthatsinglevariables approachismeaningfulandeasiertointerpret,especiallyiftheresultswillgo directlytodecisionmakers.Thresholdvaluesobtainedinmultivariateaxes alwaysrequirefurtherinvestigationsofsinglevariablesforinterpretation.Ialso agreewiththeseauthorsthattheselectionofappropriatevariablesisakey issueandvariablesreflectingtherelativefitnessoftheindividualwillbebetter thanmerelypresence/absenceorabundance(Guénette&Villard2004). Myresultsshowthatmostspeciesarepositivelyrespondingtoforestcover variables(PatchArea,HA100andSuit_Am_Habit)atlocalandintermediate scales.Inallcasesspecieswhicharenegativelyaffectedbyhabitatlossare positivelyrelatedtothesevariables(e.g. Aulacorhynchus haematopygus, Aulacorhynchus prasinus, Mionectes olivaceus, Penelope perspicax, Pharomachrus auriceps, Pyroderus scutatus, Myiodynastes chrysocephalus ).Manyotherworksreportsimilar resultsconcerningtheimportanceofhabitatamountonthemaintenanceof birdspeciesrichnessandabundance(MartínezMorales2005;Westphaletal. 2003;Trzcinskietal.1999;MazerolleandVillard1999;Villardetal.1999;

CBMMasterThesesNo.41 28 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

McIntyre1996;Bellamyetal.1996;Wilsonetal.1994;McGaricaland McComb1995),anditappearsasifthisisthereasonwhyhabitatlossisthe primarycauseofthethresholdresponseofspeciestohabitatchange(Dykstra 2004).Inmycaseandinotherstudiesaswell,manyofthosespecies,whichare consideredasahighlyvulnerablegrouptohabitatlossandfragmentation,are largebodiedfrugivorous(i.e. Aulacorhynchus haematopygus, A. prasinus, Penelope perspicax, Pharomachrus auriceps, Pionus chalcopterus, Pyroderus scutatus ;Kattan1992; Kattanetal.1994).Forinstance,accordingtomyresults, Penelope perspicax , whichisanendemicandendangeredspeciesofColombia(geographicalrange ≤50000Km2;Renjifo2001;2002),needpatcheswithatleast98hatoensure theirpresenceinfragmentedlandscapesoftheCentralAndesofColombia. Almostallspeciesnegativelyrelatedtoforestcovervariablesaresmall frugivores,whichareconsideredtobegeneralists,withmoretoleranceto habitatdisturbances(Kattan1992).Thelandscapeheterogeneityseemsto increasemobilityofmanyspeciesasacommonstrategyforsurvival(Block& Brennan1993).Then,themoreheterogeneousthehabitatmosaicis,thehigher expectedproportionofmultihabitatorgeneralistspeciesis(Kozakiewicz 1995). Myresultsshowlowresponseoffruiteatingbirdstofruitresource distribution,eventhoughIfoundsignificantcorrelationsamonglandscapes betweenfrugivorousrichness/abundanceandfruitingtreerichness/ abundance.Though Ficus, Cecropia and Miconia areimportantelementsin frugivoresdiets(Ríos2005;Luck&Daily2003;Poulinetal.1999;Loiselle& Blake1999;Loiselle&Blake1990;Estradaetal.1984;Hilty1980)atlocaland intermediatescales,theyarenotenoughtobeagoodpredictoroffrugivores birds.Theexplanationmightbethatmostfrugivorousbirdspeciesneeda broadersetofresourcestoensuretheirpresence.Forinstance,almostall speciesthatIchoseformystudyincludeintheirdietsotherresourcesbesides fruitssuchas,insects,leaves,nectar,andseeds,andinsomecases,eggsand chicks(HiltyandBrown1986;Muñoz&Kattan2007).Myresultsshowedthat increasingpatchareameansincreasingnumberofindividualsofkeyfruiting trees( Ficus, Cecropia and Miconia ),buttherelationshipbetweenbirdsandthese specificgeneraistoodiffuseanddifficulttobetrackedatspeciesspecificlevel. Perhaps,toperceiveaclearthresholdresponseinspeciespresencerelatedto foodresourcestheexplorationshouldbeduringfruitscarcityperiods,because duringtheseperiodsmajorityofspecieswillbedependingonfewkeystone species.Ifoundonlythreespeciesrelatedwithfruitresourcesdistribution.At intermediatescale Aulacorhynchus haematopygus ispositivelyrelatedwith abundanceof Ficus. Thethresholdforhighprobabilityofoccurrencewas foundtobeatleast2.25individualsof Ficus within3haofforest.Figsspecies aremainlyadaptedtointermediatesuccessionphaseofthevegetation,and somespeciesarecommonelementswithinotherkindoflandcoverssuchas forestryplantationsandasisolatedtreesingrasslandsinthesubAndean landscapes(Vargas2002).Renjifo(2001)reportsthat A. haematopygus isableto

CBMMasterThesesNo.41 29 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

useotherkindoflandcoversasforestryplantationsandgrasslands.Atlocal scale, Hemispingus superciliaris seemstobepresentinsiteswithlessthan2.5 speciesof Ficus, Cecropia or Miconia ,thiscouldbeindicatingthatthisbird speciesavoidcompetitionbyusingotherfruitresourcesandvisitsiteswithlow richnessofthesebyotherfrugivoreshighlyconsumedresources. Euphonia musica waspositivelyrelatedtotheabundanceof Miconia ,eventhougha thresholdresponsenotwasfound.Itisasmallfrugivoremainlyforaginginthe intermediatestrataoftheforest(HiltyandBrown1986). Miconia isavery commongenusinforestunderstoryandedgehabitatswithsmallandfleshy fruitswithhighwaterandcarbohydrateconcentrations,suitableforsmall bodiedanimals(Kattan1992;Vargas2002).However,theseresultswerefound atspecificscales,andfrommyresultsitisnotpossibletofindoutifthis responsealsoispresentatbroaderscales.

FrommyresultsIcansaythatforSubAndeanlandscapesinallplaceswhere wewanttoensurepresenceofspeciesnegativelyaffectedbyhabitat transformationsuchasPenelope perspicax, Pyroderus scutatus, Pionus chalcopterus, Pharomachrus auriceps, Mionectes olivaceus, and Aratinga wagleri ,patcharrangements atintermediatescaleswithnolessthan206haofsuitablehabitat(forest)with atleastonebigpatchnosmallerthan98ha,andagoodconnectivityamong patchestoenhancespeciesmovementslookingforotherresourcesandmates willberequired.Thoseresourcesmaybecomplementaryorsupplementaryto eachspecies(Dunningetal.1992;Tayloretal.1993).Itisalsoimportantthat atlocalscale,withinthe98hapatch,theheterogeneityshouldberestrictedto theforestitself(lessthan1.5kindsoflandcovers)andhasthesmalleramount ofedgeswithahighlycontrastingmatrixasitispossible(lessthan128m).For instance,for Penelope perspicax thecurrentresidentpopulationsareonlyinfew naturalpreserveareasorbigforestpatchesintheColombianAndes,andinall caseswithextensionnotlowerthan98ha(Kattan&Valderrama2006).Based onresultsfromthisstudyIcouldthinkthat P. perspicax, P. scutatus and M. olivaceus mightbeconsideredasumbrellaspecies,becausethesespeciesshowed apositiverelationwithforestcover,bothatlocalandintermediatescalesand theyneedhighamountofforesttobepresent.Probably,theproposed landscapeconfiguration,suitablefor P. perspicax, P. scutatus and M. olivaceus , alsoissuitableforotherspecieswithpoordispersalabilitysuchas Chlorochrysa nitidissima, Aburria aburri and Habia cristata (Renjifoetal.2002).However, furtherstudiesinnestednesspatternsofspeciesdiversityarerequiredto identifyifthosespeciescouldbeconsideredasumbrellaspecies. ThoughIfoundsignificantrelationshipbetweenlandscapecharacteristics,fruit resourcedistributionandsomefrugivorousbirdspeciesatlocaland intermediatescale,manyfrugivorousspeciesdidnotshowanyresponseto thosevariables.Thereasonsforthismightbelowabundanceswhichexcluded somespeciesfromtheanalysisandrestrictthestatisticalsignificance(Manelet al.2001).Somespeciesmaybeperceivingfragmentationorhabitatlossat

CBMMasterThesesNo.41 30 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

broaderscalesthanthescalesIconsidered,andotherspeciesfindthatthe landscapeconnectivityisgoodenoughtoensuretheirmovementssearching forcomplementaryandsupplementaryresources(Dunningetal.1992;Taylor etal.1993),whichmeansthattheselectedexplanatoryvariablesarenot influencingtheirstrictlypresenceonforestpatches. Mystudyhighlightstheimportanceofhabitatamount,localhabitat configurationandthelandscapearrangementatintermediatescalesforspecies conservation.Thoughforsomespeciesbigforestpatches(e.g.patchsize> 98ha)inthelandscapeseemtobecompulsorytoensuretheirpresence,small forestpatchescouldbeenoughforotherspecies(e.g. Anisognathus flavinucha or Myiodynastes chrysocephalus ,7.8ha).Howthesepatchesarearranged(landscape configuration)isoneprimaryaspecttoconsiderinlandscapeplanningand conservationstrategiestoensurepresenceofabroadspectrumoffrugivorous birdspecies(Tayloretal.2003;Turner2005). Itisanimplicitassumptioninlogisticregressionmodels,whereverspecies occursitisasuitableplaceforbreedingandnotasinkhabitat(Westphaletal. 2003)oranecologicaltrap(KristanIII2003).Forconservationpurposesthis meansthateventhoughthisstudyprovidesinformationaboutvariableswhich explainthespeciesdistributionandoccurrencethresholdsarenotenoughto ensurespeciesconservationintransformedlandscapes.Inthissense,my resultsarerelatedwiththepatternsbutmoreinformationaboutprocesses whichgeneratedthesepatternsisstillmissing.Toimprovetheconservation strategiesinmystudiedlandscapesoftheCentralAndesofColombiaitisalso necessarytounderstandthefrugivorousbirddynamicrelatedtohabitatquality, demography,resourcesavailabilityupontimeandintraandinterpatch movementcapacity.

Tomakegeneralconclusionsfromcriticalthresholdvalues(i.e.fragmentation thresholds)acrosslandscapesorregionsisdifficult,becausetheyarenot reflectingthehighvariabilityintransformedlandscapes(Lindenmayer&Luck 2005),andarereflectingtherequirementsofcommonandwidespreadspecies butnottherequirementsofthemostsensiblespecies(Mönkkönen& Reunanen1999).However,speciesspecificthresholdvaluesforfocalspecies, suchasspeciesnegativelyaffectedbyhabitattransformation,areusefultoolsas surrogateswithinaconservationstrategy.Focalspeciesmightindicate minimumrequirementsforpresenceofotherspecies,andhelpinconservation prioritize,withouttheneedfordetailedautoecologicalinformationonthose species(Hugget2005).Nevertheless,betterresultswillbeobtainedfrom thresholdvaluessupportingmanagementdecisionsifacombinationof differentspeciesresponsestodifferentvariablesandscalesisconsidered.Now, eventoughecologicalthresholdscanassistconservationstrategiestheyarenot thestrategybythemselves.Athresholdtheorymisinterpretationindecision makingprocessescouldleadtomajornegativeimplicationsforconservation

CBMMasterThesesNo.41 31 Javier Eduardo Mendoza S./Effects of Landscape Pattern and Resource Distribution on Frugivorous Bird Species in the Central Andes of Colombia: Setting Ecological Thresholds

(Lindenmayer&Luck2005).Aneffectiveconservationdoesnotmeansfit withtheminimumrequirementinsomeecologicalvariables(thresholdvalues) toensurespeciespresence,theyareanotherpiecein“theconservationpuzzle”, andforeffectivespeciesconservationinthelongrunmoreaspectsmustbe preservedsuchashabitatquality,populationandmetapopulationdynamics, landscapeconnectivity,preventinvasions,maintenanceofnaturaldisturbance regimes,andpreventnegativeimpactsinstructureandcompositionofbiotic communitiesbyhumaninhabitantsfromthesurroundings.

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Acknowledgments ManythankstomythesissupervisorsJohnnydeJongandGustavoH.Kattan, fortheirsupport,friendshipandfruitfuldiscussions.TheSwedish InternationalDevelopmentCooperationAgency(SIDA)whichgrantedme withapostgraduatescholarship.ThankstoMalinAlmstedt,Charlotta Warmark,TorbjörnEbenhard,andtheSwedishBiodiversityCentrestaff.The fieldworkwascarriedoutwithintheProject“BiodiversityandSustainable DevelopmentinColombianAndes”developedbytheAlexandervon HumboldtInstitute(AvHI),ColombiaandsupportedbyGEF,WorldBank andTheNetherlandsGovernment.SpecialthankstoFernandoGastH.,chair directoroftheAlexandervonHumboldtInstitutewhogavemefullaccessto thedataasassociatedresearcher.ManythankstoFabioH.Lozano,PaulaC. Caycedo,WilliamG.Vargas,DianaPatriciaRamirez,EderssonCabrera,Fabio LeonardoQuevedo,PedroJoséCardonaallofthemfriendsfromAvHIand involvedintheprocessesofbiologicalandspatialdatarecording.Manythanks toMarcAndréVillardforhisadviceabouttheROCanalysisforthethresholds identification.ThankstoPatricioRey.

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Appendix 1 Species of Cecropia, Ficus and Miconia and their total abundance recorded in the study areas of the Central Andes of Colombia. Abbreviation ScientificName Total Abundance Cangu Cecropia angustifolia Trecul 66 Ctele Cecropia telealba Cuatrecasas 110 Fand Ficus andicola Standley 23 Fcuat Ficus cuatrecasana Dugand 19 Fglab Ficus glabrata Kunth 32 Fhart Ficus hartwegii (Miq.)Miq. 2 Fkill Ficus killipii Standl. 12 Fmuti Ficus mutisii Dugand 10 Fsp1 Ficus sp.1 1 Fsp3 Ficus sp.3 4 Ftond Ficus tonduzii Standley 19 Fvellu Ficus velutina Willd. 1 Fyopo Ficus yoponensis Desv. 1 Macum Miconia acuminifera Tr . 95 Mcaud Miconia caudata (Bonpl.)deCandolle 54 Mcoro Miconia coronata (Bonp.)deCandolle 33 Mlehm Miconia lehmannii Cogn. 97 Mnota Miconia notabilis Triana 110 Mores Miconia orescia Uribe 1 Mresi Miconia resima Naud. 1 Msmara Miconia smaragdina Naud. 4 Msp1 Miconia sp.1 4 Msp7 Miconia sp.7 7 Msp11 Miconia sp.11 1 Msp12 Miconia sp.12 1 Msp13 Miconia sp.13 2 Msp14 Miconia sp.14 1 Msp16 Miconia sp.16 6 Msp20 Miconia sp.20 9 Msp21 Miconia sp.21 9 Msp22 Miconia sp.22 1 Mthea Miconia theaezans (Bonpl.)Cogniaux 22 Mwurd Miconia wurdackii Uribe 4

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