AmericanJournalofPrimatology72:1 - PDF document

AmericanJournalofPrimatology72:1–16(2010)REVIEWARTICLEEffectsofHabitatFragmentationandDisturbanceonHowlerMonkeys:AReviewCTORARROYO-RODRIPEDROAMERICOD.DIASCentrodeInvestigacionesenEcosistemas(CIECo),UniversidadNacionalAutonomadeMexico,Morelia,Michoacan,Me Correspondenceto:VctorArroyo-Rodrguez,CentrodeInvesti-gacionesenEcosistemas,UniversidadNacionalAutonomade r 2009Wiley-Liss,Inc. [Crockett&Eisenberg,1987;Estradaetal.,2006;Marsh,2003],butalmostallstudiesarecenteredononlyfourspecies(A.carayaA.palliataA.pigraA.seniculus).Howlershavebeencitedasarela-tivelytoleranttaxontohabitatdisturbance[e.g.Bicca-Marques,2003;Garberetal.,2006;Lovejoyetal.,1986;Schwarzkopf&Rylands,1989;VanBelle&Estrada,2006],astheyarepresentinpatcheswhereotherNeotropicalprimatespecies(e.g.spp.)cannotpersist[Estrada&Coates-Estrada,1996;Gilbert,2003].However,theymaybemoresensitivethanisusuallyconsideredtotheloss,transformationandfragmentationoftropicalforests,asallhowlerspeciesarearboreal,haveafolivore–frugivorediet,andtheirabilitytomovebetweenforestpatchesislimited,particularlywhenthesurroundingmatrixiscomposedofcattlepasturesorcroplands[Estrada&Coates-Estrada,1996;Mandujanoetal.,2004,2006].Asaprobablecon-sequenceofhabitatfragmentationanddisturbance,severalhowlerspeciesandsubspeciesareclassiedasthreatenedbytheIUCN[e.g.Vulnerable:A.palliataaequatorialis;Endangered:A.pigra;CriticallyEndangered:A.guaribaguaribaA.palliatamexicanaIUCN,2009].Therefore,itisimportanttoassessourcurrentunderstandingoftheeffectsofhabitatfragmentationanddisturbanceonhowlers.Thisreviewisfocusedonstudiesthatexplicitlyanalyzetheeffectsofhabitatfragmentationonhowlers.Nevertheless,wecomplementthereviewwithstudiesanalyzingotherhabitatdisturbanceeffects,suchasdeforestation,loggingandhunting,thatcanbefacilitatedbyhabitatfragmentation(seeFig.1).Thus,wehopethisreviewwillstimulateamorecomprehensiveunderstandingoftheecology,managementandconservationofprimatesinmod-iedlandscapes.Ouraimsinclude(1)provideasummaryoftheliterature;(2)synthesizedataonprocessesthatnegativelyaffecthowlerpopulationsinmodiedlandscapes;(3)identifyempiricalevi-dencesupportingpredictionsoftheoreticalap-proachesusedinfragmentationstudiesand(4)suggestdirectionsforfutureresearchandconserva-tionprioritiesforthistaxon.Althoughdifferentprocessesresultingfromhabitatfragmentationanddisturbancecaninteractsynergisticallytodecreasetheviabilityofprimatepopulations[seeChapmanetal.,2006],tosimplifyouranalysis,andfollowingFischerandLindenmayer[2007],wehavegroupedtheseeffectsintoexogenousandendogenousthreateningprocesses(Fig.1).Exogenousthreatsarethosethatareindependentofthespecies’biology,whereasendogenousthreateningprocessesemergeaspartofthespecies’biology.Withintheexogenousgroupofthreats,wereviewtheeffectsofchangesinhabitatpattern(e.g.decreaseinpatchsize,increaseinpatchisolation),changesinvegetationstructureandfoodavailability,andpost-fragmentationanthropogenicpressures(Fig.1).Whenconsideringendogenousthreats,themainemphasisofthisreviewisonchangesinbiology(i.e.physiologicalstressandgeneticdiversity),changesinsocialorganizationandbehavior(i.e.dispersalpatterns,groupingpatterns,socialinteractionsandactivitypatterns),andchangesinspeciesinteractions(i.e.competition,predationandparasitism). HABITAT FRAGMENTATION Spatial changes in habitat patches Number of patches Patch size Patch isolation Total Edge EXOGENOUSENDOGENOUS Anthropogenic pressuresLoggingHunting Disruptions to: Biology (e.g., physiological stress, genetic, fecundity, growth parameters) Behavior (e.g., dispersal, social system) Population decline and possibly extinction Reduction in habitat quality and food availability Species interactions: Predation Parasitism Competition Mutualisms Changes to the habitat of other species Fig.1.Deterministicthreateningprocessesarisingfromhabitatfragmentationasexperiencedbyadeclininganimalspecies.Threateningprocessesarebroadlyclassiedasexogenous(i.e.externaltoaspecies’biology)andendogenous(i.e.aspartofaspecies’biology).Anthropogenicpressuresarenotadirectconsequenceofhabitatfragmentation,butarefacilitatedbythisprocessandcanexacerbatethenegativeeffectsofhabitatfragmentationonpopulations[modiedfromFischer&Lindenmayer,2007].Am.J.Primatol.2/Arroyo-RodrguezandDias EFFECTSOFHABITATFRAGMENTATIONANDDISTURBANCEONHOWLERHabitatfragmentation[i.e.thebreakingapartofcontinuoushabitat;Fahrig,2003]isalandscape-scaleprocessthatimplieshabitatlossanditssubdivisionintoavariablenumberofpatchesdispersedinamatrixofmodiedhabitat[Fischer&Lindenmayer,2007].Typically,astheprocessofhabitatfragmentationadvances,thereisanincreaseinthenumberofisolatedorsemi-isolatedpatches,adecreaseinpatchsizeandanincreaseininter-patchdistanceandnovelhabitatboundaries(Fig.1).Habitatboundariescanvaryinstructureandcomposition,fromtheabruptboundariescomposedmainlyofcattlepastures,tomoregradualbound-ariescomposedofregeneratingvegetationatdiffer-entgrowthstages.Additionally,fragmentationmodiesthemicroclimatewithinandaroundthepatches[e.g.increaseinradiation,temperatureandwind,anddecreaseinhumidity;Saundersetal.,1991],leadingtochangesinplantcompositionandstructure.Thesechangesincludeasharplyelevatedrateoftreemortality,andalossoftreebiomass[e.g.guez&Mandujano,2006;Lauranceetal.,1997],whichcanpromotetheproliferationofyoungsecondaryvegetation,dominatedbydistur-bance-adaptedvinesandpioneertrees,andcauseaconcomitantdeclineofold-growth,forest-interiortrees[Lauranceetal.,1998].Therefore,primatesinfragmentedhabitatsareconfrontedwithahabitatofreducedsize,highlyisolatedfromotherhabitatremnants,withfewemergenttreesanddominatedbysecondaryvegetation(Fig.1).ExogenousThreateningProcessesRemovalofsuitablehabitatTheremovalorlossofhabitatisexpectedtoreduceboththedistributionrangeandpopulationsizeofagivenprimatespecies[metapopulationtheory:Hanski,1999;islandbiogeographytheory:MacArthur&Wilson,1967].Supportingthesepre-dictions,alandscape-scalestudywithA.palliataLosTuxtlas,Mexico,basedon208rainforestpatchesacrossatotalareaofca.15,000ha,showsthattheproportionofoccupiedpatchesispositivelycorre-lated(0.84)withtheabundanceofindividuals,andthatlandscapeswithagreaterproportionofsuitablehabitatcontainmoreindividuals(row1inTableI;ref5inTableII).Similarly,atthepatchscale,studiesofhowlerspeciessuchasA.palliataA.guaribaA.seniculusinseveralforesttypes,includingtropicalwet,moistanddryforests,reportthatlargerpatchescontainmoreindividualsthansmallerones,andthattheproportionofoccupiedpatches(i.e.thedistributionrange)decreaseswithpatchsize(rows2and3inTableI).Eachofthesestudiesisbasedonasamplesizeofgreaterthannineforestpatches(mean94patches)(seeTableII).Forexample,inastudyof119forestpatcheslocatedinnorthernChiapas,Mexico,Anzures-DaddaandManson[2007]ndthat19%ofthepatchesareoccupiedbyA.palliata,andthatboththenumberofindividuals(slope0.001)andoccupancy(wholemodel;0.04)arepositivelycorrelatedwithpatchsize.Asanexceptiontothesetrends,forA.palliatapopulationslivinginsixforestpatches(7–9,571ha)inCostaRica(row2inTableI;ref12inTableII),thedensityofindividualswasunrelatedtopatchsize0.21).KowalewskiandZunino[1999]alsoreportthatwhenthreeforestpatchesinArgentinaweredeforestedandreducedinsizeby32.1%,thepopulationsizeofA.carayaunchanged.Similarly,Estradaetal.[2002]studiedA.pigragroupslivingin44patches(1.9to86ha)inMexico(row2inTableI;ref14inTableII),andfoundthatforestpatcheswithandwithouthowlersdidnotdifferinsize(0.1).Thesecontrastingresultscouldbeduetothesmallsamplesizes(onlysixpatcheswerestudiedinCostaRicaandthreepatchesinArgentina),and/orthefragmenta-tionhistoryattheselocations(e.g.samplingeffects,ageofisolationandlocalhistoricalfactorssuchasrecentclearingprocesses,andhunting),whichcouldmasktheeffectofhabitatareaonhowlerpopula-tions.Forexample,Estradaetal.[2002]arguedthatthehuntinghistorycouldexplainthelackofarelationshipbetweenpatchoccupancyandpatchsize,whereasDeGamma-BlanchetandFedigan[2006]arguedthatthelargesizes(upto95.7kmofmostofthepatchestheysurveyedinCostaRicamayexplainwhythisvariablemakesnoexplanatorycontributionintheirstudy.ChangesinHabitatPatternsAnincreaseinthenumberofhabitatpatches,decreaseinpatchsizeandincreaseinpatchisolationcaninitiallyresultinarandomoccupancy(i.e.withoutaspecicpattern)oftheremainingpatches[Marsh,2003].However,overtimeprimatesmaydisappearfromsomepatchesowingtotheirsmallsizeandlimitedresources,whereastheymayrecolonizeothersuitablepatches[Chapmanetal.,2003;Mandujanoetal.,2006].Metapopulationtheorypredictsthattheprobabilityoflocalextinctioninfragmentedhabitatsincreaseswithdecreasingpatchsizeandincreasingisolation[i.e.‘‘rst-order’’factors;sensuHanski,1999],whereastheproba-bilityofcolonizationfollowstheoppositetrend[Hanski,1999].FivestudiesofA.palliataA.seniculusA.carayasupportthesepredictions(row3inTableI).Forinstance,Arroyo-Rodretal.[2008a]studied208isolatedpatches(rangingfrom0.9to266ha)inthreelandscapeswithAm.J.Primatol.ResponsesofHowlerstoHabitatModication/3 TABLEI.SummaryofBothHabitatandPopulationAttributes(HPA)AnalyzedinFragmentationStudiesWithHowlers(spp.),PredictionsTestedFromFragmentationTheory(seeText),theSpeciesAnalyzed,andEmpiricalEvidence(EE):predictionsupported;predictionnotsupported;inparentheses:indirectinferenceorrarelytestedRowsHPAPredictionsSpeciesEERefs.1LandscapeforestcoverLandscapeswithagreaterproportionofsuitablehabitatsupportmoreindividualsA.palliata2PatchsizeLargerpatchescontainmoreindividualsthansmalleronesA.palliataA.guaribaA.caraya3Thedistributionrange(%occupiedpatches)decreaseswithpatchsizeA.palliataA.seniculusA.pigra4ReducedpatchsizeandincreasedisolationresultinhigherpopulationdensitiesA.palliataA.pigraA.seniculusA.caraya5PatchisolationTheleastisolatedpatchescontainmoreindividualsthanmoreisolatedonesA.palliata6Distributionrange(%occupiedpatches)decreaseswithincreasingpatchisolationA.palliata7ShapecomplexityComplexpatchesarecolonizedmorefrequentlythancompactonesA.palliata8HabitatproductivityMoreproductivepatchesrepresentasourceofemigrantsthatmigratetowardslessproductivefragments(sinks)A.palliata)4,59FoodsourcesIndividualscanmovebetweenpatchestosupplementtheirdietA.palliataA.caraya10SmallerandmoreirregularlyshapedpatchescontainlessfoodsourcesA.palliataA.pigraA.seniculus11ChangesinvegetationaffectdistributionandabundanceofpopulationsA.palliataA.caraya12PhysiologicalstressPopulationslivinginforestpatchesaremorestressedthanthoselivinginlargeforesttracksA.palliataA.pigra13GeneticdiversityHabitatdisturbance,mainlythroughthereductionindispersionratesofindividualsbetweenpatches,reducesgeneticdiversityA.palliataA.pigraA.seniculusA.caraya30,4114SocialorganizationGroupsizedecreaseswithdecreasingpatchsizeandA.palliataA.pigraA.carayaA.seniculusA.sara15ParasitismThetransformationoforiginalhabitat,reductioninfoodavailabilityandpresenceofhumansindisturbedpatchesincreasesthevulnerabilityofindividualstoparasiteinfestationsA.palliataA.pigraA.seniculusA.caraya1.Aguilar-Cucurachietal.[2007];2.Anzures-Dadda&Manson[2007];3.Asensioetal.[2009];4.Arroyo-Rodrguezetal.[2007];5.Arroyo-Rodrguezetal.[2008a];6.Arroyo-Rodrguez&Mandujano[2006];7.Chapman&Balcomb[1998];8.Clarkeetal.[2002b];9.Clarke&Zucker[1994];10.CristoAzkarateetal.[2005];11.Chiarello[2003];12.DeGamma-Blanchet&Fedigan[2006];13.Dunn[2009];14.Estradaetal.[2002];15.Estrada&Coates-Estrada[1996];16.GarcadelValleetal.[2005];17.Gilbert[1994];18.Gilbert[2003];19.Goffardetal.[2008];20.Jamesetal.[1997];21.Juanetal.[2000];22.Lopezetal.[2005];23.Malgrem&Brush[1978];24.Mandujanoetal.[2006];25.Mandujano&Escobedo-Morales[2008];26.Mandujano&Estrada[2005];27.Marsh&Loiselle[2003];28.Martnez-Motaetal.[2007];29.McCannetal.[2003];30.Oklanderetal.[2006];31.Pope[1992];32.Rivera&Calme[2006];33.Santa-Cruzetal.[2000];34.Stuartetal.[1990];35.Terborghetal.[2001];36.Trejo-Macasetal.[2007];37.VanBelle&Estrada[2006];38.Vitazkova&Wade[2007];39.Winkleretal.[2004];40.Zuninoetal.[2007];41.Nascimentoetal.[2007];42.Kowalewski&Zunino[1989];4Zuninoetal.[2001].Am.J.Primatol.4/Arroyo-RodrguezandDias TABLEII.CharacteristicsofFragmentationStudieswithHowlersRef.SpeciesSiteMonthsGroupsDesign1ApaTuxTWF64Analyzed4smallpatches(8ha)2ApaChiTWF–23Analyzes119patches(0.2–43.4ha)ina12,500halandscape3ApaTuxTWF232Analyzes2groupsin2differentpatches(1.3–40ha)4ApaTuxTWF169Analyzes1810hapatches,9occupiedand9unoccupiedbyhowlers5ApaTuxTWF1642Analyzes208patches(0.9–266ha)in3landscapeswithdifferentforestcover6ApaTuxTWF68Analyzes15patches(1–76ha)ina4,960halandscape7Apa–TDF&–80Reviews80howlerpopulationsfromMexicotoArgentina8ApaPacTDF434Surveysa1,180hafarmwithca.25%ofremainingforestcover9ApaPacTDF130Surveysa1,180hafarmwithca.25%ofremainingforestcover10ApaTuxTWF1743Analyzes55patches(1–244ha)ina7,500halandscape11AguEspTDF––Analyzes14patches(210–35,000ha)12ApaACGTDF&6–Analyzes6patches(7–9,571ha)13ApaTuxTWF122Analyzes2groupsin2differentpatches(7.2and244ha)14ApiPalTWF1018Analyzes44patches(1.9–86ha)15ApaTuxTWF–60Analyzes126patches(2–1,000ha)and44agriculturalsites16ApiLacTWF3–Analyzesacontinuousforestand3patches(1–1,700ha)17AseManTMF1613Analyzes310haand2100hapatches,andacontinuousforest18AseManTMF––Analyzesacontinuousforestand9patches(1–100ha)19AsaSanTWF1223Analyzespopulationsofareserveand3cattleranches20ApiCBSTMF210Analyzesapopulationlivinginhighlydisturbedconditions21ApaTuxTWF63Analyzes3patches(3.2–250ha)22AseLagTDF93Analyzes2islands(0.6and190ha)23ApaPacTDF917Surveysa1,180hafarmwithca.25%ofremainingforestcover24,25ApaTuxTWF2817Analyzes92patches(1–76ha)inaca.4,960halandscape26ApaTuxTWF–36Analyzes130patches(0.5–150ha)in2landscapeswithdifferentforestcover27ApiCBSTMF126Analyses6patchesoccupiedandoneunoccupiedbyhowlers(1.3–75ha)28ApiT&CTMF84Analyzes2patches(2ha)andtwositesincontinuousforest29ApaFllTDF897Analyzescoffeeplantations(25–225ha)30AcaCorTDF––Analyzes9patches31AseHatTDF–18Analyzes2populationsinhabitingalargecattleranch32ApiCalTDF85Analyzes2sitesina700,000haforestreserveand2patches(11.6and13.9ha)outsidethereserve33AcaC&CTDF––Analyzes44individualsin3areaswithdifferentfragmentationdegree34ApaPac&20Analyzesa450haforestedfarmandacontinuousforest(50,000ha)35AseLagTDF–14Analyzes6small(0.25–0.9ha),4medium(4–12ha)andtwolargeislands(150ha),and2sitesinmainland(350ha)36Apa&Tux&TWF12110Analyzes6protectedforests(1,400haeach)and6patches(1–40ha).37ApiM>DF&–120Analyzes5largepatches(850–2,700ha)and3reserves(57,600–700,000ha).38ApiM&BTWF&79Analyzes5patches(80ha)and4continuousforests(100ha)39Apa&N&BTDF34Analyzes3groupsofA.palliatainanislandandonegroupofA.pigralivinginapatches40AcaCorTDF434Analyzes24patchesina4,500halandscape41AcaB&BTWF––Analyzes4sites,threeinBrazilandoneinBolivia42AcaCorTDF–3Analyzes3patchesbetween1984and199543AcaC&MTDF–61Analyzes5sitesWeindicatethestudyspecies(Aca,Alouattacaraya;Agu,A.guariba;Apa,A.palliata;Api,A.pigra;Asa,A.sara,Ase,A.seniculus),studysites,habitattype,numberofmonths,numberofgroups,andstudydesign.ReferencenumberscorrespondtothoseinTableI.Sites:AreadeConservacionGuanacaste,CostaRica(ACG);SeverallocationsinCentralBrazilandonesiteinBolivia(B&B);Calakmul,Campeche(Cal);Chiapas,Mexico(Chi);CommunityBaboonSanctuary,BermudianLanding,Belize(CBS);CorrientesandChacoProvinces,Argentina(C&C),CorrientesProvince,Argentina(Cor);CorrientesandMisionesprovinces,Argentina(C&M);EspirituSanto,Brazil(Esp);FincaLaLuz,MombachoVolcano,Nicaragua(Fll);HatoMasaguaral,LosLlanos,Venezuela(Hat);Lacandonrainforest,Mexico(Lac);LagoGuri,Venezuela(Lag);Manaus,Brazil(ManSeveralplacesinshouternMexicoandBelize(M&B);ShouternMexicoandnorthernGuatemala(M&G);IsladeOmetepe,Nicaragua,andtheScotlandHalfMoonarea,Belize(N&B);LaPacica,CostaRica(Pac);Palenque,Chiapas,Mexico(Pal);LosTuxtlas,Mexico(Tux);SantaCruz,Bolivia(San);StofTabascoandCampeche,Mexico(T&C).Habitats:Werecognizedthreebroadvegetationtypesbasedonannualrainfall:tropicalwetforest(TWF),tropicalmoistforest(TMF)andtropicaldforest(TDF)[Gentry,1982].Am.J.Primatol.ResponsesofHowlerstoHabitatModication/5 differencesinforestcover(rangingfrom4to24%),andfoundthatpatchsizewasthebestpredictor(withapositiveeffect)ofpatchoccupancybyA.palliataineachlandscape.Similarly,patchsizehasbeenconsistentlydescribedasthebestpredictorforpopulationsize[Cristobal-Azkarateetal.,2005]andviability[Mandujanoetal.,2006]ofA.palliatainLosTuxtlas(refs.10and24inTableII).Thefactthatpatchisolationisnotastrongpredictorofpatchoccupancycouldbeduetoanumberofmethodolo-gicalproblemsassociatedwiththemetricsusedtodeneanddescribepatchisolation[seeArroyo-guez&Mandujano,2009].Nearlyallfragmen-tationstudieswithhowlersusedistance-basedisolationmetricssuchasthedistancetothenearestpatch.Thisisolationmetriccanunderestimatetheeffectsofisolationbecauseitdoesnotconsiderthepresenceofverysmallvegetationremnants(step-pingstones),livefencesandotherelements(e.g.isolatedtrees)inthematrix,whichcanprovidefoodandfacilitateinter-patchmovements[e.g.Arroyo-guez&Mandujano,2009;Asensioetal.,2009].Futurestudiesshouldtesttheeffectsofisolationbyusingarea-basedisolationmetrics,suchastheamountofavailablehabitatwithinagivenradiusofapatch,asthesemetricsareamorereliablemeasureofpatchisolation[Arroyo-Rodrguez&Mandujano,2009].EvidencefromA.palliataA.pigra,A.seniculusA.carayaintropicaldryandwetforestsindicatesthatpopulationdensitycanincreaseinsmallerandmoreisolatedpatches(row4inTableI).Thus,howlersmayberesistanttotheinitialphasesofdisturbance,andconcentrateinasmallnumberofisolatedforestpatches[e.g.Estradaetal.,2002;Rosales-Medaetal.,2007].Theregulatoryeffectthatnaturalpredatorshaveonhowlerpopulationsmaybelessintenseinfragmentedhabitats,aslargepredators(e.g.HarpiaharpyjaPantheraonca)areusuallyamongtherstanimalstodisappearfromdisturbedareas[e.g.Terborghetal.,2001].Thisabsencehasbeensuggestedasafactorcontributingtotheinitialorshort-termhighpopulationdensitiesofhowlerslivinginsmallpatches[Chiarello,2003;Gilbert,2003;Lovejoyetal.,1986;Terborghetal.,2001].Theproliferationofhighlyproductivesecond-aryvegetationinsmallpatcheshasbeensuggestedasanadditionalfactorthatcouldhelptomaintainhighpopulationdensitiesinsmallpatches[e.g.Kowalewski&Zunino,1999;Lovejoyetal.,1986].Althoughpopulationslivingathighdensitiesmayrespondbettertostochasticthreats,particularlywhenpopulationsarelarge[Fischer&Lindenmayer,2007],enduringhighdensitiescouldhavenegativeconsequencesforthelong-termpersistenceofhow-lers[seethe‘‘ChangestoSpeciesInteractions’’Changesinthehabitatpattern(e.g.decreaseinpatchsize,increaseinpatchisolation)arerelatedtotwoprocessesthatmayexplainthedistribution,abundanceandinter-patchmovementsofhowlerpopulationsinfragmentedlandscapes[Dunningetal.,1992]:landscapesupplementationandsource/sinkrelationships.Landscapesupplementationoc-curswhenanimalsuseanumberofneigh-boringpatchesbecausetheycontainsupplementaryresources.Forinstance,whenapatchisverysmallbutisalsoveryclosetoanotherpatch(es)withsupplementaryresources,individualsmayusesev-eralpatchestomeettheirdietaryrequirements(row9inTableI).Forexample,Zuninoetal.[2007]observedvegroupsofA.carayausingmorethanoneforestpatchseparatedbygrasslandsinnorthernArgentina,andthesegroupsoccupiedthesmallestpatches(5ha)inthearea.Asimilarpatternofmulti-patchusewasobservedbyMandujanoetal.[2006]andAsensioetal.[2009]ingroupsofA.palliatainhabitingverysmallpatches(3ha)inLosTuxtlas,Mexico.Theseobservationshighlighttheabilityofhowlersbothtoexploitsmallforestpatchesandtomovebetweenisolatedforestpatches[alsoseePozo-Montuy&Serio-Silva,2007],andagreewiththefrequentlycitedbehavioralexibilitythatisthoughttoallowhowlerstocopewithhabitatdisturbance[e.g.Bicca-Marques,2003].Neverthe-less,whenhowlersarerequiredtodescendtotheground,theyfaceanincreaseinpredationriskfromdogs[Pozo-Montuy&Serio-Silva,2007]andotheranimals(seethe‘‘ChangestoSpeciesInteractions’’Source/sinkrelationshipsoccurwhenamoreproductivepatchrepresentsasourceofemigrantsthatmigratetowardlessproductivepatches,usuallynamedsinks[Pulliam,1988].Assinkpatcheshaveinsufcientfood,populationslivinginsinksmaygoextinctwithoutimmigrationofindividualsfromsourcepatches.Source/sinkdynamicsmaybeatworkinhighlyfragmentedlandscapesoccupiedbyA.palliataatsitessuchasLosTuxtlas,Mexico,assomegroupsarelivinginpatchesthatdonotpresentthecharacteristicsrequiredfortheirlong-termsurvival(e.g.theyareverysmall,highlyisolatedandwithfewlarge(DBH60cm)treesandfewfoodplantspecies)(row8inTableI;refs.4and5inTableII).Inthesestudies,ithasbeensuggestedthatsuchpatchesmayfunctionallybesinks,asithasbeenarguedforotherprimatespecies[e.g.Procolobusrufomitratus:Mbora&Meikle,2004].Habitatfragmentationcanalsoincreasethetotalamountofhabitatboundariesthroughtheincrementoftheperimeter-to-arearelationship(i.e.shapecomplexity)ofthepatches.Patchshapecomplexityoffersadvantagesanddisadvantagestohowlersinfragmentedlandscapes.Forexample,complexlyshapedpatchescanbecolonizedmoreeasilythancompact(e.g.round)patchesduetothefactthattheyhaveaproportionallygreateramountofedge,increasingthelikelihoodthatapatchwillbeAm.J.Primatol.6/Arroyo-RodrguezandDias encounteredbyamovingindividual,eitherbychance[Ewers&Didham,2006]ordeliberately[Boinski&Garber,2000].ThishypothesishasbeenusedtoexplainwhypatchoccupancybyA.palliatawaspositivelyrelatedtobothpatchsizeandshapecomplexityinalandscapedominatedbylivefencesandvegetationcorridorsinLosTuxtlas,Mexico(row7inTableI).However,aswedescribebelow,irregularlyshapedpatchesexperiencehigheredgeeffects,affectingplantcompositionandvegetationstructurewithinthepatch,whichcouldinturndecreasefoodavailabilityforhowlers.ChangesinvegetationattributesandfoodavailabilityFoodavailabilityinpatchesdependsonpatchsize,homerangesizeandthecompositionandstructureofvegetation.StudiesofofviewedbyBicca-Marques,2003]andparticularlyA.palliatapalliata´bal-Azkarate&Arroyo-Rodr2007]haveshownthathomerangesizedecreaseswithdecreasingpatchsize(0.01,respectively),limitingtheamountofresourcesavailabletoeachgroup.However,asmallhomerangedoesnotalwaysresultinlowfoodavailability[seeGillespie&Chapman,2001].ThisdependsonthespeciccompositionoftheforestTwomainprocessesaffectthevegetationinpatches,namely,samplingeffectsandedgeeffects[i.e.environmentalchangesnearpatchedges;Saundersetal.,1991].Althoughsamplingeffectsresultindifferentpatternsofthepresence/absence/dominanceofparticularspeciesinremnants,en-vironmentalchangesalterplantcompositionandvegetationstructurewithinthepatches.Usuallytheseenvironmentalchangesresultinhighermor-talityratesoflargeold-growthtreespeciesnearpatchedges[Lauranceetal.,1997],decreasingtreebiomassinthesmallestandmostirregularlyshapedpatches[e.g.Arroyo-Rodrguez&Mandujano,2006].Changesinvegetationstructurethatcanreducefoodavailabilitytohowlersinpatchesincludethelossofemergenttrees[Arroyo-Rodrguez&Mandujano,2006;Dunnetal.,2009;Juanetal.,2000;Rivera&,2006]andthereductionofplantspeciesrichness[Arroyo-Rodrguez&Mandujano,2006;Juanetal.,2000;Lopezetal.,2005;row10inTableI].Thesepatternshavebeenreportedfortropicalwet,moistanddryforests(refs.6,21,22,27and32inTableII).Forexample,afteranalyzingthetopfoodplantspecies(i.e.thosecontributingoffeedingtime)ofA.palliatainLosTuxtlas,Arroyo-guez&Mandujano[2006]foundthatthebasalareaoftheseplantspecieswasnegativelyrelatedtopatchsize(0.01).Similarly,Loetal.[2005]analyzedthevegetationoftwoislands(0.6and190ha)inhabitedbyA.seniculusinLagoGuri,Venezuela,andreportedthatthenumberofplantspeciesfoundonthesmallerisland(46species)washalfthenumberfoundonthelargerisland100species).Thechangesinvegetationinhighlyfragmentedhabitatsmayaffectthedistributionandabundanceofhowlers.Thepresenceandabundanceofhowlershavebeenpositivelycorrelatedwiththediversity,abundanceandbasalareaofimportantfoodre-sources(row11,TableI).Nevertheless,itisstillunclearwhichofthesevegetationattributeshasthegreatestinuenceonhowlerpopulations.Althoughbal-Azkarateetal.[2005]andEstradaandCoates-Estrada[1996]showthatplantspeciesdiversityisrelatedtothepopulationsizeofA.palliatainLosTuxtlas,Mexico,Arroyo-Rodretal.[2007]andAnzures-DaddaandManson[2007]demonstratethatthedensityoflargetreesisthebestpredictorofthedistributionofA.palliatainLosTuxtlasandChiapas,Mexico.Furtherstudiesarenecessarytoidentifywhichattributeshavethelargestinuenceondifferenthowlerpopulationsindifferentforesttypes,ascurrentevidencecomesalmostexclusivelyfromstudieswithA.palliatatropicalwetforests(TablesIandII).Thisinforma-tionhascriticalimplicationsforhowlerconservationinalteredhabitats.PostfragmentationanthropogenicpressuresAnthropogenicpressures(e.g.logging,hunting)arenotadirectconsequenceofhabitatfragmenta-tion,butcanbefacilitatedbythisprocess,exacer-batingthenegativeeffectsofhabitatfragmentationonpopulations(Fig.1).Poachingandcapturingliveprimatesforpetshavebeenconsideredtwoofthemostimportantthreatsforprimatesurvivalinfragmentedhabitats[Chapman&Peres,2001;Oates,1996;Peres,2000],largelybecauseprimatesmaybemorevulnerabletopoachersinthesmallestandmostaccessiblesites[Chiarello&deMello,2001;Peres,1990,2001].HuntingmayhavehadanimportantnegativeeffectonhowlerpopulationspopulationsA.caraya:Agoramoorthy&Lohmann,1999;A.guariba:Chiarello&Galetti,1994;A.palliataDuarte-Quiroga&Estrada,2003;A.pigra:Wattsetal.,1986;A.sara:Goffardetal.,2008;A.seniculusPeres,1990,2000,2001],butitshouldbenotedthattheeffectsofhuntingonhowlersmaybecontext-dependent.Forinstance,inCentralAmazonia,Brazil,howlersareintensivelyharvestedformeat[e.g.Peres,2000],whereasatotherlocationssuchasLosTuxtlas,Mexico,peopleonlyoccasionallyhuntthemforthepettrade[V.A.R.&P.A.D.D,pers.obs.].Therefore,theimpactofhuntingonhowlerswillvaryasafunctionoflocalhistoricalandsocio-economicfactors.However,itremainstobedemonstratedwhetherhuntingratesarehigherinfragmentedforests.Am.J.Primatol.ResponsesofHowlerstoHabitatModication/7 Thepostfragmentationextractionofforestpro-ductscanleadtoadditionallossoffoodresourcesimportanttohowlers(Fig.1).Forexample,inLosTuxtlas,Mexico,theinhabitantsoftenremoveunderstoryplantstoallowthecattletoenterthepatches[Arroyo-Rodrguez&Mandujano,2006].Treefellingalsohasbeenobservedinthisandotherregions,wherelocalpopulationslogwoodspeciessuchasAlbiziapurpusii(Rubiaceae)andsp.(Araucaria-ceae)tobuildtheirhousesandforfuel[Arroyo-guez&Mandujano,2006;Kowalewski&Zunino,1999;Zuninoetal.,2007].Thesetreesareamongthemostcommontreesinthehowlerdiet[Bicca-Marques,2003;Cristobal-Azkarate&Arroyo-guez,2007].However,nostudiestodatehavedirectlyquantiedtheeffectsofloggingonhowlerpopulationsizes,structureorpersistence.Afewstudieshaveattemptedtoindirectlymeasuretheseeffects[Arroyo-Rodrguezetal.,2008a;Kowalewski&Zunino,1999;Zuninoetal.,2007].Forinstance,guezetal.[2008a]foundthatsmallpatcheslocatedatgreaterdistancesfromvillagesaremorelikelytobeoccupiedbyA.palliatathanarelargerpatcheslocatednearertovillages,andarguethatthispatternmayberelatedtologging.Furtherstudiesrelatingdifferentintensitiesofselectiveloggingtopopulationsizes,structureandpersistencearenecessarytoassesstowhatextentloggingaffectshowlerpopulations.EndogenousThreateningProcessesInadditiontotheexogenousthreateningpro-cessesdescribedabove,thedistributionandpopula-tionstructureofhowlersinfragmentedhabitatsmaybeaffectedbychangesintheirbiology,behaviorandinteractionswithotherspecies(Fig.1).AsFischerandLindenmayer[2007:269]noted,‘‘thesechangesareoftentriggeredbyexogenousthreats,butmayconstitutethreateningprocessesintheirownright.’’ChangesinbiologyBiologicalchangeshavebeenreportedforhowlerslivinginfragmentedhabitats,includingincreasedphysiologicalstressandlossofgeneticdiversity(rows12and13inTableI).Forinstance,inarecentstudyofA.pigra,16individualslivinginforestpatcheshadsignicantlyhigherlevelsofstress(asmeasuredinfecalcortisol)than17individualslivinginacontinuousforest,suggestingthatphysio-logicalstressmayincreaseasaresultofforestfragmentation[Martnez-Motaetal.,2007;TablesIandII].Similarly,Dunn[2009]reportsthatfecalglucocorticoidconcentrations(ameasureofstress)arehigher(127.131.5ng/g,meanSD)amonganA.palliatagroupofsixindividualsinhabitingasmall(7.2ha)forestpatch,thaninagroupofsixindividualsinhabitingalarger(244ha)patch18ng/g).Theincreaseinthenumberofsolitarymaleslivinginisolatedpatcheshasalsobeensuggestedtoresultinanincreaseintheconcentrationoftestosterone,formales,andcortisol,forfemales,inapopulationofA.palliatapalliata´bal-Azkarateetal.,2006,2007].Ashigherlevelsofbothhormonesincreaseenergeticdemands,andfoodavailabilityisexpectedtobereducedinsmallerandisolatedpatches(seeabove),individualslivinginfragmentedhabitatsmayexperiencecompromisednutrition,fecundityandsurvivorship.Additionalstudiesontheeffectsofhabitatfragmentationonphysiologicalstressarenecessarytoassesshowthisfactoraffectsthehealth(e.g.parasiteincidence)andpersistenceofwildpopula-tions.Thisinformationiscriticaltoidentifyfactorssinglyandincombinationthatmayaffectthesurvivalofprimatesinfragmentedlandscapes[seeChapmanetal.,2006,2007].Forinstance,crowdinginsmallpatchesmayleadtohigherratesofaggression,whichinturncouldleadtoincreasedsocialstress[Honess&Marin,2006].Underthesecircumstances,higherstresslevelsinindividualslivingindisturbedhabitatscouldbeabyproductoffragmentation,ratherthanadirectconsequenceofit.Othernegativeconsequencesofpopulationiso-lationareinbreedingandgeneticdrift.Bothpro-cessesaremoreintenseinsmallerpatches,astheseusuallyhavesmallerpopulations,andresultinlowergeneticdiversity.Theeffectsoftheseprocessesmayreducetheresponsecapacitiesofindividualstonaturalorhuman-inducedchanges[Jumpetal.,2009].AlthoughstudiesofA.carayaA.palliataA.pigraA.seniculussuggestthathabitatdisturbance—mainlythroughthereductionindis-persalratesofindividualsbetweenpatches—couldreducegeneticdiversity(row13inTableI;refs.20,23,30,31and41inTableII),recentstudiesconductedwithA.pigrapopulationslivinginfragmentedhabitatsfoundhigheraveragehetero-zygosisthanthatreportedinpreviousstudies(refs.16and39inTableII).Thismaybeassociatedwithdifferencesinthemethodologiesusedineachstudy,thesmallsamplesizesorwiththerecentseparationofthepopulations,andsuggeststhatfurtherlong-termgeneticstudiesarerequiredtodemonstratetheeffectofisolationonthegeneticdiversityofhowlerpopulations.ChangesinsocialorganizationandbehaviorHabitatfragmentationcanalsoleadtodisrup-tionstothesocialorganizationandbehaviorofhowlerssuchaschangesin:(1)dispersalpatterns;(2)groupingpatterns;(3)socialinteractions;and(4)activitypatterns.Aspatchesbecomesmallerandmoreisolated,howlers’abilitytodispersesuccess-fullydecreases.Quantitativedataonmaleandfemaledispersalpatternsinredhowlers[e.g.Am.J.Primatol.8/Arroyo-RodrguezandDias Crockett&Pope,1993]andmantledhowlers[e.g.Clarke&Glander,2004]areavailable.However,littleisspecicallyknownconcerningthemovementofindividualsbetweenparticularforestpatches,thefrequencyofsuchevents,theroutesthatareused,orthecriteriausedbyhowlerstoselectwhichpatchtodisperseto.Althoughthereareseveralobservationsofhowlerstravelingontheground[A.palliataAsensioetal.,2009;Clarkeetal.,2002a;Estrada&Coates-Estrada,1996;A.pigra:Crockett,1998;Pozo-Montuy&Serio-Silva,2007],theirdispersalabilitiesindisturbedmatricesarelikelyrestricted.Specically,studieswithfragmentedpopulationsA.palliataA.pigrainMexicosuggestthattheremaybeisolationthresholdsthatlimitdispersalbetweenpatchesalongtheground.Thesethresholdsmayvaryasafunctionofthemortalityriskassociatedwithlongdistancetravel,energeticcostsandpredation[Mandujano&Escobedo-Morales,2008;Mandujano&Estrada,2005;Mandujanoetal.,2004;VanBelle&Estrada,2006].Theconstraintsassociatedwithlimiteddispersalfromsmallandisolatedpatchesmayresultinincreasesinpopulationdensity[e.g.A.pigra:VanBelle&Estrada,2006],andinbreedingandlossofgeneticvariability[A.palliata:Arroyo-Rodrguezetal.,A.guariba:Fortes&Bicca-Marques,2008].Wecouldnotidentifyaclearpatternintheeffectsofhabitatfragmentationonthesizeandcompositionofhowlergroups.AlthoughvestudiesA.pigraA.palliatashowthatgroupsizetendstodecreasewithdecreasingpatchsize,nosuchrelationshipwasfoundinotherhowlerpopulationsA.carayaA.palliataA.seniculusA.sara;row14inTableI).Regardinggroupcompositionandsocialinteractions,evidenceisonlyavailablefromstudiesanalyzinghabitatdisturbanceeffects.Forinstance,inmoredisturbedhabitats,denedashabitatstransformedbyanthropogenic(e.g.logging)ornatural(e.g.hurricanes,droughts)events,thenumberofmalespergroupislowerandtheproportionofunimalegroupsincreases[A.palliataClarkeetal.,2002a,b;McCannetal.,2003;A.pigraEstradaetal.,2002;VanBelle&Estrada,2006;A.seniculus:Rudran&Fernandez-Duque,2003].Inaddition,ssion–fusiondynamics[denedastem-poralvariationinspatialcohesionandindividualmembershipinagroupovertime;seeAurelietal.,2008]becomemoreprevalent[A.palliata:Dias&guez-Luna,2005,2006],andboththeratesofsocialinteractions[0.010interactions/ind/hrvs.0.004interactions/ind/hr:Clarkeetal.,2002a]andtheproportionoftimespentinsocialactivity[1.2%vs.0.55%:Behie&Pavelka,2005]decrease.Overallthesedataindicatethathabitatdisturbancemayaffectthesocialorganizationofhowlers;however,otherstudiesofA.palliata[Mandujano&Escobedo-Morales,2008],A.caraya[Zuninoetal.,2007]andA.sara[Goffardetal.,2008]disputethispossibility.Thus,furtherstudiesspecicallydesignedtomea-suretheeffectsoffragmentationongroupcomposi-tion,socialinteractionsandsocialorganizationareneeded[seeArroyo-Rodrguez&Mandujano,2009].Changesintheactivitypatternsofindividuals(i.e.proportionofdailyactivityspentresting,feedingandmoving)havebeenreportedinrelationtohabitatdisturbanceandfragmentation.Clarkeetal.[2002a]foundthatafterthepartialdeforesta-tionoftheirhomerange,agroupof10adultmantledhowlersincreasefeedingtimefrom18to22.3%,possiblytocompensateforreductioninfoodavailability.Asensioetal.[2007b]observedthatagroupof59mantledhowlerslivinginanareaofextremelyhighpopulationdensity(9.5ind/ha)spentagreateramountoftimefeedingandtraveling(29vs.24%and14vs.6%,respectively)andreducedtimespentresting(55%vs69%),relativetoanothergroupofsixhowlersthatlivedinasmall(1.3ha)patchatlowerdensity(4.6ind/ha).Incontrast,Juanetal.[2000]observednodifferencesinactivitypatternsamongthreegroupsofA.palliatalivinginhabitatsofdifferentsizes.Similarly,intheirmeta-analysisofthedietandactivitypatternsofA.palliatainLosTuxtlas,bal-AzkarateandArroyo-Rodrguez[2007]foundthatneitherpatchsizenorpopulationdensityhadasignicanteffectontheactivitypatternsofhowlers.Similarly,afterexaminingallstudieswithhowlers(withduration9months),Bicca-Marques[2003]reportedthatactivitypatternsdidnotvarywithpatchsize.Thesecontrastingresultssuggesthowlerscanexploithabitatsthatvaryinsize,degreeofdis-turbance,isolationandpopulationdensitywithrelativelyminoradjustmentsinthetimetheyengageinfeeding,travelingandresting.Inthisregard,anevaluationofhabitatquality,withspecicemphasisonthepresence,abundanceandnutritionalcontentsofimportantplantspeciesinthehowlers’diet,willhelpinterpretne-grainedvariationinactivitypatterns.Finally,howleractivitybudgetsseemtobeconstrainedbyenergy-savingbehavioraladapta-tions,associatedwithrestingandrelatedtotheirdigestivephysiology[Milton,1998].Thus,perhapshowlers’abilitiestomodifytheiractivitypatternsarelimited,inwhichcasenutritionalstressisexpectedtoparticularlyaffectpopulationslivinginthelessproductivehabitatsandhabitatslackingpreferredplantspecies.Unfortunately,westilldonotknowhowoverallshiftsinsocialorganization(e.g.increasesintheproportionofunimalegroupsinpopulations)andbehavior(e.g.reductionindispersalrates)ofhowlersareaffectedbyhabitatfragmentation.Long-termstudiesofA.palliataA.seniculusthatwhentheamountofhabitatincreases,howlerpopulationstendtoexpand,mainlythroughtheformationofnewgroups,whichareusuallysmallAm.J.Primatol.ResponsesofHowlerstoHabitatModication/9 andunimale[Fediganetal.,1998;Rudran&ndez-Duque,2003].Theseimportantndingsindicatehowhowlerpopulationsrespondtoin-creasesinforestcover,butdonotnecessaryexplainthelong-termresponseofhowlerpopulationsandgroupstohabitatlossandfragmentation.ChangestospeciesinteractionsChangesinspeciesinteractionsincludecompeti-tion,predationandexposuretoparasites(Fig.1).Asindicatedabove,populationdensityusuallyincreasesinthesmallestpatches,andthiscouldincreaseintra-speciccompetition.Highpopulationdensitieshavebeenassociatedwithreductionsinfoodavail-abilityandtheexploitationofalternativenontreefoodresources[Cristobal-Azkarate&Arroyo-guez,2007;Rodrguez-Lunaetal.,2003].Forexample,Rodrguez-Lunaetal.[2003]observedthataftersignicantpopulationincrease(from1.2ind/hato6.9ind/ha),apopulationofmantledhowlersbegantointensivelyexploitalternativefoodsources(mainlylianasandvines;from8.8%offeedingtimeto21%)andthedurationoffeedingboutstendedtodecrease(from3.1to2.1min).Similarly,bal-Azkarateetal.[2005]speculatethatimmaturemortalityinafragmentedpopulationofA.palliata(43groupslivingin15fragments)increasedathighpopulationdensities,asnoneofthepopulationslivingatdensitieshigherthan0.71ind/hahadjuveniles.Theseauthorsproposethatthistrendispossiblymediatedbylowerfoodavailabilityunderhigh-densityconditions.Therealsoisevidencethatreproductionissuppressedinhowlerpopulationslivingatdensitiesof10ind/haind/haA.seniculus:Terborghetal.,2001].Terborghetal.[2001]reportthatona0.6haisland,agroupofhowlerscontainingtwoadultfemales(populationdensityof10ind/ha)producedonlyoneyoungin4years(0.125birthperfemale-year),whereasona350haisland,10adultfemalesbelongingtotwogroups(0.3ind/ha)producedveinfantsinasingleyear(0.5birthperfemale-year).Finally,increasedinter-andintra-speciccompetitionoverfoodisexpectedtooccurinsmallerpatches,wherefoodresourcesarelimitedandfeedingencountersmaybemorecommon[Dias&Strier,2000;Roseetal.,2003;Stevensonetal.,2000].However,thereisonlyweakevidencefortheoccurrenceofdirectinter-andintra-speciccompetitionforfoodinhowlers[butseeAsensioetal.,2007a;Cristoetal.,2004].Althoughhabitatfragmentationmaynegativelyaffectthepresenceoflargepredatorpopulations,thesesamehabitatsareoftencharacterizedbyanincreaseinthenumberofwildmid-levelpredators(e.g.coyotes,foxes)and/ordomesticdogsandcats[e.g.Crooks&Soul,1999;May&Norton,1996].Althoughthishypothesisneedsfurtherinvestiga-tion,primatesareexpectedtobemorevulnerableinopenenvironments,suchasthosepresentinfrag-mentedlandscapes[Santamara,2004].Forinstance,Pozo-MontuyandSerio-Silva[2007]andCamargoandFerrari[2007]observedacoyote(Canislatransandfourtayras(Eirabarabara),respectively,attack-ingajuvenileofA.pigraandasubadultfemaleofA.belzebul,respectively,travelingontheground.Similarly,Ludwigetal.[2007]arguethatthepresenceofhowlers(A.caraya)insuccessionalvegetationwithalowforestcanopycanfacilitatethepredationbycougars(Pumaconcolor).EstradaandCoates-Estrada[1996]andPavelkaetal.[2003]alsoarguethathabitatdisturbancepromotedbyfragmentationandhurricanes,respectively,mayforcehowlerstotravelontheground,increasingtheirpredationriskfromterrestrialpredatorssuchasboasanddogs.Atopicofgrowingconcernisthepotentialeffectofemerginginfectiousdiseases(EIDs)onendan-geredprimatepopulations[Nunn&Altizer,2006].Forinstance,thetransformationoforiginalhabitat,increaseofinbreeding,reductioninfoodavailability,thepresenceofhumansanddomesticatedanimalsindisturbedpatches,orevensomemanagementac-tions,suchasthebuildingofcorridorsconnectingforestfragments,mayincreasethevulnerabilityofindividualstoEIDsinfestations.InA.palliataA.carayaA.seniculushigherendoparasiteloadshavebeenrelatedtohigherpopulationdensityinsmallpatches[Aguilar-Cucurachietal.,2007;Gilbert,1994;Santa-Cruzetal.,2000;Stuartetal.,1990],andinA.carayaA.palliataA.pigraparasiteprevalenceishigherinindividualslivinginfragmentedhabitats(prevalence:A.carayaofindividualsinfected;A.palliata45.7%;A.pigra24.0%)comparedwithmorecontinuousforestA.caraya7.14%;A.palliata23.7%;A.pigra13.0%)[Santa-Cruzetal.,2000;Trejo-Macasetal.,2007].Inaddition,severalgroupsofA.pigrawereinfectedwithaparasite(Giardiaduodenalis)mostprobablytransmittedtothemthroughhumanfeces[Vitazkova,2009;Vitazkova&Wade,2007].Itispossiblethat,asshownforP.rufomitratus[Chapmanetal.,2007],parasitismco-varieswithtemporaluctuationsinfoodabundance,andforhowlerpopulationslivingindisturbedhabitatsthiscouldleadtodecreasesinthetnessofinfectedindividuals.Todate,nostudyhasdemonstratedconclusivelythatsuchchangesinhost–parasitedynamicsaredetri-mentaltohowlers.CONCLUSIONSANDFUTUREDIRECTIONSAcomplexpictureaboutourcurrentunder-standingoftheeffectsofhabitatfragmentationanddisturbanceonhowlersemergesfromthisreview.HowlersareamongthemoststudiedNeotropicalprimatetaxa[e.g.DiFiore&Campbell,2007],andAm.J.Primatol.10/Arroyo-RodrguezandDias manyeffortshavebeendirectedtowardstudyinghowlersinfragmentedanddisturbedhabitats.Thus,theinformationwehaveforhowlersallowsustodevelopbestmodelingapproachesofprimatere-sponsestohabitatfragmentationanddisturbance.Howlersareknownfortheirabilitytopersistinbothconservedanddisturbedhabitats,includingnaturallyfragmentedlandscapes[e.g.A.seniculusLosLlanos,Venezuela;Brazaetal.,1981]andverysmallforestpatches(5ha)whereotherprimatespeciescannotsurvive[Chiarello,2003;Estrada&Coates-Estrada,1996;Lovejoyetal.,1986].Never-theless,inourreview,wefoundevidenceindicatingthathabitatlossnegativelyaffectsthedistributionandabundanceofhowlers.Inparticular,studiesA.carayaA.guaribaA.palliataA.pigraA.seniculusindicatethatpatchsizeisanimportantfactornegativelyaffectingthepresence,abundanceandpersistenceofhowlerpopulationsinfragmentedhabitats.Thus,weproposethathabitatlossprobablyhaslargerconsistentnegativeeffectsonhowlerpopulationsthanhabitatfragmentationperse[seeFahrig,2003].Habitatareaispositivelyrelatedtofoodavailability[e.g.Arroyo-Rodrguez&Mandujano,2006;Cristobal-Azkarate&Arroyo-guez,2007],andnegativelyrelatedtoanthropogenicpressures[e.g.Peres,2000,2001],physiologicalstress[e.g.Martnez-Motaetal.,2007]andparasiterisk[e.g.Gilbert,1994].Therefore,webelievethatthemostimportantmanagementre-commendationsforhowlerpopulationsindisturbedhabitatsaretoincreasetheremaininghabitatareaandtoconservethelargesthabitatremnants.Inlargerhabitatsthenegativeeffectsofshapecomplexity(e.g.edgeeffects)arelower,whereasthepositiveeffects(e.g.increasedpatchaccessibility)arehigher(seethe‘‘ChangesinHabitatPatterns’’section).Thereductionofpopulationsizesinsmallerforestpatchescouldnegativelyaffecthowlers’persistence.Smallpopulationsaremoresusceptibletostochasticthreateningprocessessuchasdiseaseepidemics[Agostinietal.,2008;Nunn&Altizer,2006],environmentalcatastrophes(e.g.hurricanes)anddemographic(e.g.year-to-yearvariabilityinreproductivesuccess)andgenetic(e.g.geneticdrift)stochasticity[Cowlishaw&Dunbar,2000;Fischer&Lindenmayer,2007;Gilpin&Soule,1986].Addition-ally,threateningprocessesusuallyhavethepotentialtointeractwith,andmagnifytheeffectsofeachother,creatingwhathavebeendescribedas‘‘extinctionvortices’’[Gilpin&Soule,1986].Thus,althoughthehighresilienceand‘‘pioneer’’capacityspp.[Bicca-Marques,2003;Garberetal.,2006;Lovejoyetal.,1986;Schwarzkopf&Rylands,1989;VanBelle&Estrada,2006]mayallowthemtosurviveinhighlyimpactedhabitats,thecurrentrateofhabitattransformationassociatedwithhumanactivities[countrieslikeBolivia,BrazilorEcuadorhadannualratesofforestlostintheperiodof1990–2005ofmorethan0.5%;FAO,2007]willeventuallyresultinlocalextinctionofmanyhowlerInthissense,amajorfocusoffuturestudiesshouldbetheidenticationofthresholdvaluesforhabitatamountunderwhichthelong-termpersis-tenceofindividualhowlerspeciesandpopulationswillbecompromised[e.g.Andren,1994].Thesedatahaveimportantmanagementimplicationsforen-dangeredprimates,althoughitisimportanttohighlightthatitismoreresponsibletorequiregovernmentstousereferencevaluesforhabitatamountswellaboveminimumthresholds(i.e.resi-liencethinking).Inaddition,landscape-scalestudiesofferthemosteffectivemeansofdeterminingmanage-mentpolicies[Arroyo-Rodrguez&Mandujano,2009].ThisapproachhasbeenappliedinastudywithA.palliatainthreefragmentedlandscapesinLosTuxtlas,Mexico[Arroyo-Rodrguezetal.,2008a].Inthisstudy,itwasdeterminedthatboththeproportionofoccupiedpatchesandtheabundanceofprimatesdecreasedsignicantlyinlandscapeswithlessthan15%ofremaininghabitat,suggestingthatpopulationpersistencecouldbecompromisedinthelongterminhighlyfragmentedlandscapes[Arroyo-Rodretal.,2008a].Foroneoftheselandscapes,itwasestimatedthatwithanannualdeforestationrateof4%,thepopulationofA.palliatahadanextinctionprobabilityof35%inthenext30years[Mandujanoetal.,2006].Nevertheless,if112–170haarerestoredinthis5,000halandscape,byconnectinglargepatcheswithlowpopulationsizes,theauthorspredictthattheextinctionprobabilitywoulddropto1%.Thisexampleillustrateshowthepersistenceofhowlersinalteredlandscapesdependsonthemanagementactionspromotedoverthecomingyears.Ourreviewrevealsthatpatchisolationisnotastrongpredictorofeitherpatchoccupancyorpopulationsizeforhowlers.Aswediscussedinthetext(seethe‘‘ChangesinHabitatPatterns’’section),thiscouldberelatedtoanumberofmethodologicalproblemsofthemostcommonlyusedisolationmetrics[seeArroyo-Rodrguez&Mandujano,2009].However,thisresultcouldalsoreecttheabilityofhowlerstomoveamongpatches,highlightingtheecologicalplasticityoftheseprimates.Forexample,anumberofstudieswithA.palliataA.pigraA.carayareportthathowlerscantravelontheground,alonglivefences,andotherlandscapeelementssuchasisolatedtrees,andthatsomegroupscansupplementtheirdietsbymakinguseofresourcesfromseveralforestpatches[e.g.Asensioetal.,2009;Pozo-Montuy&Serio-Silva,2007].Infact,wefoundseveralpapersindicatingthathowlersmayberesistanttotheinitialphasesofdisturbanceandconcentrateinasmallnumberofisolatedforestpatches,inwhichotherprimatespecies(e.g.cannotpersist[e.g.Estrada&Coates-Estrada,1996;Gilbert,2003].Amongotherfactors,thesuccessofAm.J.Primatol.ResponsesofHowlerstoHabitatModication/11 howlersincopingwithhabitatdisturbancehasbeenrelatedtotheircapacityto(1)feedfrommanydifferentplantspeciesandadapttheirdiettothespeciesavailableinthehabitat[e.g.Pintoetal.,2003;Rivera&Calme,2006],(2)increasetheamountofleavesintheirdiet[Asensioetal.,2007b;Juanetal.,2000;Rodrguez-Lunaetal.,2003],(3)consumeexoticandsecondaryspeciesfrequentindisturbedhabitats[Bicca-Marques&Calegaro-Marques,1994],(4)usesmallhomeranges[Estrada&Coates-Estrada,1996;Lovejoyetal.,1986]and(5)utilizeenergy-savingactivitybudgets[Milton,1998].Wefoundhoweverthatinseveralotherareasourcurrentknowledgeis,atbest,fragmentary.Amongthese,wehighlighttwo.First,wearelackingdirectquanticationoftheeffectsofpostfragmenta-tionanthropogenicpressures,suchashuntingandlogging,onhowlerslivinginpatches.Althoughmanystudieshavesuggestedthathuntinghasstrongdetrimentaleffectsonhowlerpopulations[e.g.Chiarello&Galetti,1994;Duarte-Quiroga&Estrada,2003;Goffardetal.,2008;Peres,2000],wecannotcurrentlydeterminehowfragmentationfacilitatesthepenetrationofhumanhuntersinpatches.Furthermore,severalstudieshavespecu-latedthatselectiveloggingandwoodextractionareaffectingtheavailabilityoffoodresourcestohowlers,butnostudieshavedirectlyanalyzedthisassertion.Actually,itisstillunclearwhichvegetationattri-buteshavethebiggestinuenceonhowlerpopula-tions.Vegetationcompositionandstructuremaybestronglyrelatedtopatchsize,shapeandisolationandhence,theinuenceofvegetationonhowlersshouldbeevaluatedthroughdesignsthatallowdiscriminationbetweentheeffectsofhabitatspatialpatternsandthoseofvegetationperse.Weshoulddothiswithseveralhowlerspecies,indifferenthabitattypes,andinlandscapeswithdifferentlevelsofSecond,regardingtheendogenousthreateningprocesses,evidenceforhowthedistributionandpopulationstructureofhowlersinpatchesarebeingaffectedbychangesintheirbiology,behaviorandinteractionswithotherspeciesisvague.Forin-stance,additionalstudiesareneededtoassesstowhatextentincreasesinphysiologicalstressofindividualsinhabitingsmallpatchesaffectstheirhealth(e.g.parasiteincidence)andpopulationpersistence.Similarly,inthefuture,itwillbeimportanttoconductlong-termstudiesonpopula-tiongeneticstoevaluatethepossibilitythatalossofgeneticdiversityhasalreadyoccurredinfragments.Additionally,theimpactofEIDsmustbeinvesti-gatedmorethoroughly.Inparticular,weneedtoimproveourmeasuresofdiseasepresenceinnaturalandmodiedhabitats.Wealsoneedtodevelopmodelstopredicthowhost–parasitedynamicswillchangeinresponsetoclimatechange,andhowwillthisaffectthesurvivalofhowlerpopulations.Finally,itisimportanttohighlightthattheinformationpresentedinthisarticlecomesalmostexclusivelyfromfour(A.carayaA.palliataA.pigraA.seniculus)ofthetenspeciesofhowlerscurrentlyrecognized[Cortes-Ortizetal,2003],andthatvirtuallynothingisknownabouttheeffectsofhabitatfragmentationonA.belzebulA.coibensisA.guaribaA.macconelliA.nigerrimaA.saraAssomeofthesespeciesinhabithighlydisturbedareasinSouthAmerica—likeA.guaribainBrazilianAtlanticforests—intheshort-termresearcheffortsmustbedirectedtowardassessmentsofthecurrentstatusoftheirhabitats,populationdynamicsandbehavioralecology.Additionally,futurestudiesshouldassessinter-specicdifferencesinspecies’responsestohabitatlossandfragmentation.Ashowlerspeciesdifferingroupsizeandcomposition[Bicca-Marques,2003;Chapman&Balcomb,1998;Crockett&Eisenberg,1987]andinhabitdifferenthabitats(fromtropicalwettotropicaldryforests),theirresponsestohabitatalterationareexpectedtovary[Ewers&Didham,2006].WethankJ.Fischerforallowingustouseamodiedversionofhispublishedgure.J.Fischer,J.Cristobal-Azkarate,J.Dunn,A.Rangel-NegrL.A.Escobedo-Morales,S.Aguilar-Cucurachi,P.Garberandtwoanonymousreviewersprovidedmanyusefulcommentsandsuggestionsthatgreatlyimprovedthemanuscript.Finally,wethankJ.DunnforeditingthenalversionofthemanuscriptinEnglish.ThisresearchadheredtotheAmericanSocietyofPrima-tologistsethicalguidelinesforthetreatmentofnon-humanprimatesandwasconductedinaccordancewiththelegalrequirementsoftheInstitutodeEcologaA.C.,Depto.BiodiversidadyEcologaAnimal,Veracruz,andthecountryofMexico.AgoramoorthyG,LohmannR.1999.Populationandconserva-tionstatusoftheblack-and-goldhowlermonkeys,,alongtheRioRiachuelo,Argentina.NeotropPrimates7:43–44.AgostiniI,HolzmannI,DiBitettiMS.2008.Infanthybridsinanewlyformedmixed-speciesgroupofhowlermonkeysAlouattaguaribaclamitansAlouattacaraya)innorth-easternArgentina.Primates49:304–307.Aguilar-CucurachiMS,Canales-EspinosaD,Paez-RodrguezM.2007.ParasitosgastrointestinalesenmonoaulladorAlouattapalliata)enlaregiondeLosTuxtlas,Veracruz,xico.In:Bicca-MarquesJC,editor.AprimatologianoBrasil,Vol.10.PortoAlegre,RS:SociedadeBrasileiradePrimatologia.p225–237.nH.1994.Effectsofhabitatfragmentationonbirdsandmammalsinlandscapeswithdifferentproportionofsuitablehabitat:areview.Oikos71:340–346.Anzures-DaddaA,MansonRH.2007.Patch-andlandscape-scaleeffectsonhowlermonkeydistributionandabundanceinrainforestfragments.AnimConserv10:69–76.Am.J.Primatol.12/Arroyo-RodrguezandDias 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