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J Appl Ecol 20191ndash12 wileyonlinelibrarycomjournaljpe emsp|emsp1copy 2019 The Authors Journal of Applied Ecology copy 2019 British Ecological Society
Received11April2018emsp |emsp Accepted14January2019DOI1011111365-266413360
R E S E A R C H A R T I C L E
Measuring the surrogacy potential of charismatic megafauna species across taxonomic phylogenetic and functional diversity on a megadiverse island
Marsya C Sibarani1 emsp| Moreno Di Marco23 emsp| Carlo Rondinini4 emsp| Salit Kark1
1TheBiodiversityResearchGroupTheSchoolofBiologicalSciencesCentreforBiodiversityampConservationScienceTheUniversityofQueenslandBrisbaneQLDAustralia2CentreforBiodiversityandConservationScienceTheUniversityofQueenslandBrisbaneQLDAustralia3CSIROLandampWaterBrisbaneQLDAustralia4GlobalMammalAssessmentProgramDepartmentofBiologyandBiotechnologiesSapienzaUniversitagravediRomaRomeItaly
CorrespondenceMarsyaCSibaraniEmail marsyachrgmailcom
HandlingEditorJohanduToit
Abstract1 ConservationorganisationsandgovernmentsoftenusecharismaticmegafaunaassurrogatestorepresentbroaderbiodiversityWhilethesespeciesareprimarilyse-lectedasldquoflagshipsrdquoformarketingcampaignsitisimportanttoevaluatetheirsur-rogacypotentialietheextenttowhichtheirprotectionbenefitsotherbiodiversityelementsFourcharismaticmegafaunaspeciesareusedassurrogatesinthemegad-iverseislandofSumatratheSumatrantigerPanthera tigris sumatraeSumatranel-ephantElephas maximus sumatranusSumatranorangutanPongo abeliiandSumatranrhinoceros Dicerorhinus sumatrensisWeexaminedhowwelleachofthesespeciesperformedinrepresentingthedistributionofallco-occurringterrestrialmammalspeciesontheislandandthepriorityareasfortheconservationofthreefacetsofmammalianbiodiversity(taxonomicphylogeneticandfunctional)
2 Weusedhabitat suitabilitymodels to represent thedistributionof 184 terrestrialmammalspecies160phylogeneticgroupsand74functionaltraitgroupsWethenidentifiedpriorityconservationareasusingthespatialprioritisationsoftwareZonation
3 Wefoundthatthehabitatoverlapbetweeneachofthefourcharismaticspeciesandtheothermammalspeciesvariedrangingfromameanof52(SD=27)forthetigerto2(SD=2)fortherhinoCombiningthefourspeciestogetherimprovedtherepresentationlevelsonlymarginallycomparedtousingthetigeronlyAmongthefourcharismaticmegafaunaspeciestheextentofsuitablehabitatofSumatrantigercoveredthehighestproportionofpriorityconservationareasTheSumatrantigeralsooutperformedmostofothermammalspecieswithsimilarrangesizes
4 Wefoundthatsomeofthetop-rankedconservationareasfortaxonomic(28)phylogenetic(8)andfunctionaldiversity(19)didnotoverlapwithanyofthecharismaticspeciesrsquosuitablehabitat
5 Synthesis and applicationsWide-rangingcharismaticspeciescanrepresentbroadermammalianbiodiversitybuttheymaymisssomekeyareaswithhighbiodiversityimportanceWesuggestthatacombinationofsystematicspatialprioritisationandsurrogacyanalysesareimportantinordertodeterminetheallocationofconser-vationresourcesinbiodiversity-richareassuchasSumatrawhereanexpansionoftheprotectedareanetworkisrequired
2emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
1emsp |emspINTRODUC TION
Conservingallbiodiversity featuresat thesametime isnot feasi-bledue to limited resourceshenceconservationeffortsmustbestrategically planned and prioritised (Bottrill etal 2008 JosephMaloneyampPossingham2009)Oneconservationstrategythat isoftenapplied is toemployaspeciesorgroupofspecies inmanycaseslargeandcharismaticspeciesasflagshipsAflagshipspeciesisldquoaspeciesusedasthefocusofabroaderconservationmarketingcampaign based on its possession of one ormore traits that ap-pealtothetargetaudiencerdquo(VerissimoMacMillanampSmith2011)Howevermostofthecampaignsprimarilyseekfundsdirectlyforthe flagships and are rarely aimed to benefit other biodiversity(Smith Veriacutessimo Isaac amp Jones 2012) Considering limited re-sourcesforconservationandthevastrangeofbiodiversitythatre-quireprotectionconservingflagshipspeciesintheirnaturalhabitathasagreatpotentialtocontributetothepersistenceofbiodiversitywhen properly planned
Whileflagshipspeciesdonotnecessarilyactasumbrellaspe-cieswhoseconservationconfersprotectiontoa largenumberofco-occurring species (Roberge amp Angelstam 2004)mdashcharismaticmegafaunamayserveasbothflagshipandumbrella (Caro2010)However previous work has shownmixed results as to whethercharismaticmegafaunaspeciesareeffective surrogates forbiodi-versityAndelmanandFagan(2000)reportedlittleevidencefortheeffectivenessofvarious surrogateschemes includingcharismaticspecies for regional species conservation in the United StatesSimilarlyWilliams Burgess and Rahbek (2000) found that areasidentifiedbasedonthedistributionofflagshipspeciesdonotper-form better in representing the diversity of mammals and birdsthanareas identifiedfromrandomlyselectedspecies Incontrastconservation networks for jaguarPanthera onca in LatinAmericarepresentsubstantialproportionofhigh-qualityhabitatsforotherterrestrial mammals (Thornton etal 2016) and the giant pandaAiluropoda melanoleucaisaneffectivesurrogateforendemicmam-malandbirdspeciesinChina(LiampPimm2016)InAfricathepri-ority conservation areas for theAfrican ldquoBig Fiverdquo species highlyrepresentpriorityareas for theothermammals yetprovidepoorrepresentations for amphibians reptiles invertebrates andplants(DiMininampMoilanen2014)
Mostevaluationsofsurrogatespeciesfocusedontheirrepresen-tationof taxonomicdiversityHowever taxonomicdiversity alonedoes not capture other important facets of biodiversity such asphylogeneticdiversitymdashthedistinctivenessamongspeciesbasedon
their evolutionary history (Faith 1992)mdashand functional diversitymdashthedistributionofspeciesinamultidimensionalnichespacedefinedbytheirlife-historytraits(PetcheyampGaston2006)Thislimitstheglobalunderstandingofsurrogacypotentialforcharismaticspeciesbecausedifferentfacetsofbiodiversityoftenshownon-congruentspatialpatternsForexampleglobalmammalhotspotsdefinedusingtaxonomic phylogenetic and functional diversity are not spatiallycongruent(Mazeletal2014)Similarlythereisonly46overlapamongthetoppriorityconservationareasformammalconservationacrossthethreefacets(Brumetal2017)Onacountryscalefunc-tionaldiversityofbirdsinFranceisunderrepresentedinprotectedareas whereas taxonomic diversity is overrepresented (Devictoretal2010)
SumatraisapartoftheSundalandbiodiversityhotspotwheretheuseof charismaticmegafauna to guide conservationeffortsis a common practice (Ministry of Forestry of the Republic ofIndonesia2007PHKA2015SoehartonoSusiloAndayanietal2007 Soehartono Susilo Sitompul etal 2007 SoehartonoWibisonoetal2007)TheprotectedareacoverageofSumatrarequiresanexpansionfromthecurrent~11ndash17toachievethecommitmentssetundertheConventiononBiologicalDiversitysAichi Target 11 assuming proportional allocation to land areaacross the major islands in Indonesia Conservation efforts inSumatra have been largely targeted towards four charismaticmegafauna species the Sumatran tigerPanthera tigris sumatraetheSumatranelephantElephas maximus sumatranustheSumatranorangutanPongo abeliiandtheSumatranrhinocerosDicerorhinus sumatrensis Conservationists often propose that these largemammalshaveanumbrellaeffectandthatsavingthemwillalsosaveanumberofotherco-occurringspeciesHoweverthispro-claimedumbrellaeffectremainslargelyuntestedespeciallywhenitcomestomultiplefacetsofbiodiversitysuchasfunctionalandphylogeneticdiversityInthisworkweaddressedthisimportantshortfallandevaluatedwhethertheavailablehabitatforfourflag-shipspeciesinSumatraisrepresentativeofthetaxonomicfunc-tional and phylogeneticmammal diversity (hereafter ldquosurrogacypotentialrdquo)
Our firstaimwas tomeasure thehabitatoverlapbetweenthefourcharismaticspeciesofSumatraandtheothernativeterrestrialmammalspeciesontheislandThesecondaimwastoidentifythepriority areas formammal conservation in Sumatra based on tax-onomic phylogenetic and functional diversity and to assess howmuch these areas would benefit from the protection of the fourcharismaticspecies
K E Y W O R D S
functionaldiversityphylogeneticdiversityspatialconservationprioritisationSumatranelephantSumatranorangutanSumatranrhinocerosSumatrantigersurrogatespecies
emspensp emsp | emsp3Journal of Applied EcologySIBARANI et Al
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy region
Sumatra isoneofthe largest islands in Indonesiawithatotalareaof430000km2 (GADM2009)The island is surroundedbymanysmallersatelliteislandsyetthisstudyfocusedonlyonthemainis-land (Figure1) Forest landuse zones aredivided into three func-tionsbiodiversityconservation(106oftheisland)watersystemprotection (13) and production (356)Other land uses (408of the island) include agriculture land and settlements (MargonoTurubanova Zhuravleva Potapov amp Tyukavina 2012) Between1990 and 2010 an estimated 75million hectares of primary for-estinSumatrawereclearedand23millionhectareshavebeende-graded leavingonly30ofSumatracoveredbyprimaryforest in2010 (Margonoetal 2012)ThehumanpopulationofSumatra in2010was506millionwithagrowthrateof145between2000and2010(BadanPusatStatistik2012)
22emsp|emspMammal distribution data
We obtained the list of native terrestrial mammal species inSumatrausing(a)thesearchtoolonIUCNRedListofThreatenedSpecieswebsite(wwwiucnredlistorg)and(b)theIUCNgeographicdistributionrangesforterrestrialmammals(IUCN2016)Becausethetwolistsdidnotreturnthesamenumberofspecieswemerged
themandcheckedthespeciesinformationpagesontheIUCNRedListwebsitetofilterspeciesthatoccurinSumatra(excludingspe-ciesthatonlyoccuronsatelliteislands)Thisresultedin193mam-malspeciesbeinglisted includingthefoursurrogatespecies(seeAppendixS1)
Giventhe lackofcomprehensiveoccurrencedata fordevelop-ingstatisticaldistributionmodelsforallspeciesweuseddeductive(expert-driven)habitatsuitabilitymodels to representspeciesrsquodis-tributions on the island (Rondinini etal 2011) Habitat suitabilitymodelshavebeenusedinanumberofotherstudiesonaregional(egThorntonetal2016)andglobalscale(egBrumetal2017)wherecomprehensiveoccurrencedatawereunavailableRondininietal(2011)assessedspeciesrsquohabitatsuitabilitybyconsideringspe-cieshabitatpreferencesforthreeenvironmentalvariablesthetypesoflandcoverelevationrangeandhydrologicalfeaturesTheresult-ingdeductivemodelsconsistof threeclassesofhabitatsuitability(Rondininietal2011)
i Highhabitat suitability representing theprimaryhabitatwherethespeciescanpersist
iiMediumhabitatsuitabilityrepresentingsecondaryhabitatwherethespeciescanbefoundyetcannotpersistwithouttheprimaryhabitatand
iiiLowhabitatsuitabilityrepresentingareaswherethespeciesaregenerallynotfoundorunlikelytooccur
F IGURE 1emspMapofthestudyregionSumatraIslandSmallinsertmapshowsthelocationoftheislandinIndonesia
4emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
In the spatial prioritisation analysis we only used areas of highhabitat suitability to represent theoccurrenceof the species (here-after ldquoextent of suitable habitatrdquo) becausewe intendedwanted theresulting conservation area systems to include areaswhere speciesaremost likelytopersistOfthe193nativeterrestrialmammalspe-cies inSumatra thetworecentlysplitorangutanpopulations (Nateretal2017)wereconsideredasonespeciesandeightspecieswerenotmodelledbyRondininietal(2011)thereforeouranalysisincludedatotalof184species(includingthefourcharismaticspecies)
23emsp|emspAssessing the representation of mammal species by the charismatic megafauna
Weassessedthesurrogacypotentialofcharismaticmegafaunaspe-cies by overlaying their extent of suitable habitatwith that of allothermammals Representationwas calculated as the proportionof a speciesrsquo extent of suitable habitat overlappingwith thehabi-tatofeachcharismaticmegafaunaspeciesWeperformedall spa-tialdataprocessingusing therpackages ldquosprdquo (PebesmaampBivand2005)andldquorasterrdquo(HijmansampvanEtten2012)inrversion341(RDevelopmentCoreTeam2008)
24emsp|emspAssessing the representation of priority areas based on multiple facets of biodiversity
We identified conservation priority areas using the Zonation v4software(Moilanenetal2014)TheinputdataforZonationanaly-sisarerastermapsofbiodiversityfeatures(egspeciesandhabitattypes)whichrepresenttheirspatialdistributionTheZonationalgo-rithmstarts from the full extentof the landscapeof interest andtheniterativelyremovesareaswiththelowestvalueforconserva-tionbasedontheoccurrencelevelofbiodiversityfeatures(Moilanenetal2005)Thisiterativeremovalprocessgeneratesamapshow-ing a hierarchic ranking of conservation priorities throughout thelandscape(MoilanenKujalaampLeathwick2009)Eachrastercelloftheoutputmap contains a rankof conservationpriorities rangingbetween0(lowestpriority)and1(highestpriority)thatcanbevisu-alisedasahierarchicalzonedmapoftoppriorityareasforconserva-tionZonationhasalreadybeenusedforassessingumbrellaeffectsofsurrogatespecies(DiMininampMoilanen2014)andexaminingcon-gruencyofpriority areas formultiple facetsofbiodiversity (Brumetal2017PollockThuillerampJetz2017StreckerOldenWhittierampPaukert2011)
We used Core Area Zonation as the cell removal rules inZonationwhichranksthecellsacrossthe landscapebasedonthemost importantoccurrenceof a feature andhencecould identifycore areas of features in biodiversity-poor areas (Moilanen etal2014)We also incorporated connectivity considerations by usingthe Boundary Length Penalty to produce more compact reservesolutions (MoilanenampWintle2007)We ran three separate anal-yses to identify priorities for threedifferent biodiversity facets aspecies-level analysis (taxonomic prioritisation) an analysis basedonphylogeneticgroups(phylogeneticprioritisation)andananalysis
basedonfunctionalgroups(functionalprioritisation)Furthertech-nicaldetailsareprovidedinAppendixS2
25emsp|emspBiodiversity features for spatial prioritisation
Weusedindividualspeciesasthebiodiversityfeaturesforthespa-tialprioritisationbasedontaxonomicdiversityWeperformedarea-weighted resampling to scaleup thehabitat suitabilitymaps fromtheoriginal300mresolutionto1kmWeusedaresolutionof1kmas a compromise between computational time and relevance forconservationmanagement on the islandWeweighted14 speciesendemictoSumatratwiceasmuchasthenon-endemicspeciestorepresentthehigherglobalvalueoftheirconservationontheislandWealsoperformedasensitivityanalysisonalternativeweightingofendemicspeciesbuttheresultsshowednosubstantialdifferences(seeAppendixS4)
For spatial prioritisation based on phylogenetic diversity wedefined phylogenetic groups following the framework developedbyStreckeretal(2011)andBrumetal(2017)Weusedthemam-malian phylogenetic supertree created by Bininda-Emonds etal(2007)andupdatedbyFritzBininda-EmondsandPurvis(2009)tocreateaphylogeneticdistancematrixamong181mammalspeciesinSumatraafterexcludingthreespecieswhichwerenotavailablein themammaliansupertreeWethenperformedprincipalcoordi-nateanalysisonthephylogeneticdistancematrixandselectedthefirst16eigenvectorswhichexplainedgt1oftotalvariationTheseeigenvectors altogether accounted for 69 of the total variationEacheigenvectorwassplitinto10quantiles(seeAppendixS4forthesensitivitytest)andthenconverted intobinaryvariablesOurquantileswerewiderthanthoseusedinBrumetal(2017)becausewe had fewer number of species in Sumatra To represent phylo-geneticgroups inspatialmapswecreatedabinarymatrixofspe-ciestimesphylogeneticgroupArea-weightedhabitatsuitabilitymapsat1kmresolutionwerereclassifiedintobinarymapswithathresholdof005 (this threshold reduces the riskof introducingcommissionerrorswithoutpenalisingspecieswithnarrowhabitatdistributions)andthenwereconvertedintogridtimesspeciesmatrixFinallywemul-tipliedthetwomatricestoobtaingridtimesphylogeneticgroupsmatrixinwhichagridcellcontainedthenumberofspeciesbelongingtoaparticularphylogenetic groupWe thengenerated spatialmapsofphylogeneticgroupdistributionfromthismatrix
Wemappedmammalianfunctionaltraitswithsimilarprocedurewithphylogeny-basedprioritisationusing life-history traitsasop-posed to phylogenetic eigenvectorsWe selected five life-historyand ecological categories represented by nine traits adult bodymassmaximumlongevityreproductivespeed(weaningagegesta-tionlength)reproductionoutput(neonatebodymasslittersizeandlittersperyear)andresourceuse(trophiclevelandhabitatbreadth)WeusedtheglobaldatasetforterrestrialmammaltraitscompiledbyPacificietal (2013)andDiMarcoandSantini (2015)fromvarioussourcessuchasPanTHERIA(Jonesetal2009)andAnAge(Tacutuetal2013)Weassignedthepresenceabsenceofeachlevelofcate-goricaltraitsinabinarymatrixofspeciestimestraitWesplitcontinuous
emspensp emsp | emsp5Journal of Applied EcologySIBARANI et Al
traitsinto10quantilesandweassignedpresenceabsenceofeachsame-sizetraitleveltospeciesNextwemultipliedthegridtimesspe-ciesmatrixwithspeciestimestraitmatrixWeconvertedtheresultingmatrixofgridtimestraitintospatialmapsoffunctionaltraitlevelsThedetailedprocedureofdatapreparationisprovidedinAppendixS2
Werantheprioritisationanalysisseparatelyusingspeciesrsquohabi-tatsuitabilitymapsasinputsintaxonomy-basedprioritisationphy-logeneticgroupmapsinphylogeny-basedprioritisationandlevelsoffunctionaltraitsintrait-basedprioritisationWethenextractedthe
top51017and25ofpriorityareasforeachprioritisationscenariosandoverlaid themwith theextentof suitablehabitatofthecharismaticmegafaunaspeciesWemeasuredthesurrogacypo-tentialofcharismaticmegafaunaastheproportionofpriorityareasacrossSumatrathatoverlappedwiththeextentofsuitablehabitatofthespeciesunderconsiderationInadditionwealsocalculatedthesurrogacypotentialsofothermammal species inSumatra tocom-pare the performance of the four charismatic megafauna specieswiththatofotherspecies
F IGURE 2emspTherepresentationoftheco-occurringmammalspecieswithinthesuitablehabitatofcharismaticmegafauna(a)overalland(b)categorisedaccordingtotheirIUCNRedListcategoriesDDDataDeficientLCLeastConcernNTNearThreatenedVUVulnerableENEndangeredCRCriticallyEndangeredNotethatthescalesofy-axisof(b)aredifferentacrossthefourcharismaticmegafaunaspecies
TigerE
lephantO
rangutanR
hinoceros
0 25 50 75 100
0
50
100
150
0
50
100
150
0
50
100
150
0
50
100
150
Representation ()
Num
ber o
f spe
cies
Tiger Elephant Orangutan Rhinoceros
0 25 50 75 100 0 25 50 75 0 20 40 60 80 0 3 6 9
DD (N = 13)
LC (N = 110)
NT (N = 20)
VU (N = 26)
EN (N = 12)
CR (N = 3)
Representation ()
IUC
N R
ed L
ist c
ateg
orie
s
(a)
(b)
6emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
3emsp |emspRESULTS
31emsp|emspSurrogacy for terrestrial mammal species
Among the four charismaticmegafauna species the tiger had thehighest spatial overlap with other mammal species represent-ingameanof52 (SD=27)of theextentof suitablehabitatofother Sumatranmammals (Figure2) The representation levels forothercharismatic speciesweremuch lower18 for theelephant(SD=12) 9 for the orangutan (SD=11) and 2 for the rhi-noceros(SD=2)Onlytwospecieshadahighspatialoverlapwiththeelephant(ie93forthelesserlarge-footedmyotisMyotis has-seltii and85 for thebig-earedhorseshoebatRhinolophus macro-tis)Likewiseonly twospecieshadahighspatialoverlapwith theorangutan(ie81forthebig-earedhorseshoebatand71forthepen-tailedtreeshrewPtilocercus lowii)
Mostofthesuitablehabitatfororangutanandrhinocerosover-lappedwiththetigerbutonly41oftheelephantsextentofsuit-ablehabitatoverlappedwiththetigersThesuitablehabitatfortigeroverlappedsubstantially(52)withthecriticallyendangeredSundapangolin Manis javanica Of the 12 endangered species (Figure2)onlyonewasunderrepresentedbythetigeriethehairy-nosedotter
Lutra sumatranawithrepresentationlevelof12Theother11en-dangeredspecieswerewellrepresentedbythetigerwiththeover-laprangingfrom40to89Combiningthefoursurrogatespeciesonlyimprovedtherepresentationlevelsbyameanof5(SD=6range=0ndash12)comparedtotheperformanceofthetigeralone
32emsp|emspSurrogacy for priority areas based on multiple facets of biodiversity
Wediscoveredsubstantialspatialmismatchesamongtheareasiden-tifiedundertaxonomicphylogeneticandfunctionaldiversityprior-itisation scenarios (Figure3)When looking at the top5priorityareasforeachbiodiversityfacetswhichaltogetherencompassedanareaof21595km2we foundanoverlapofonly3227km2 (15)acrossthethreefacetsPriorityareassharedamongthethreeprior-itisationscenariosmostlyoccurredinhighlandsofnorthernSumatraandwesternmountainrangesIntaxonomy-basedprioritisationthepriorityareasweremorespreadoutacrosstheislandincludingcen-tral lowlandandeasterncoastsThespatial solution forprioritisa-tionbasedonphylogeneticgroupswasmoreclumpedinthewesternhalfoftheislandPriorityareasforconservingfunctionaltraitswere
F IGURE 3emspPriorityconservationareasinSumatrabasedonmultiplefacetsofbiodiversityThetopmapsreportthespatialprioritisationresultsreportingtherankingofconservationprioritythroughoutthelandscape(with0meaninglowestimportanceand1meaninghighestimportance)WecategorisedhighpriorityareasintofourgroupsofnestedpriorityrankingsTop5(valuesofgt095)top10(gt090)top17(gt083)andtop25(gt075)Theinsetmapsreportthespatialdistributionofcharismaticmegafaunaspecies
Priority rankingTop 5Top 10Top 17Top 25
Taxonomic diversity Phylogenetic diversity Functional diversity
Maps of charismaticmegafauna species
Tiger Elephant Orangutan Rhinoceros
0 400200 km
Extent of suitable habitat
emspensp emsp | emsp7Journal of Applied EcologySIBARANI et Al
morecongruenttophylogeny-based(20overlap)thantaxonomy-basedprioritisation(17overlap)
Ingeneralmostoftheextentofsuitablehabitatofthecharis-maticspecieswasofhighconservationpriority(Figure4)Theorang-utanandrhinoceroscoveredareasinSumatrawithrelativelyhigherconservationpriorityranksthanthetigerandelephantAmongthefour elephant had the most variability in representing conserva-tionprioritiesegfortaxonomicprioritisationIQRelephant=044
IQRtiger=023 IQRorangutan=010 IQRrhinoceros=005 (com-pletesummarystatisticsinAppendixS4)
Whilemostofthesuitablehabitatsfortheorangutanandrhinoc-erosoverlappedwithareasofhighconservationprioritytheseonlyac-countedforsmallproportionoftoppriorityareasgiventherestricteddistributionofthesespecies(Figure5)Thetigerssuitablehabitathadthehighestarealcoverageofpriorityareasforthethreebiodiversityfac-etsanditrepresentedphylogeneticprioritiesparticularlywellElephant
F IGURE 4emspBoxplotsshowingthevariationofconservationpriorityrankswithintheextentofsuitablehabitatofcharismaticmegafaunaspecies The y-axisrepresentstheconservationpriorityranksthatwerecomputedbasedoniterativecellremovalprocessofZonationrangingfrom0(lowestpriority)to1(highestpriority)
Taxonomic diversity Phylogenetic diversity Functional diversity
Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino
000
025
050
075
100
Charismatic megafauna
Con
serv
atio
n pr
iorit
y (0
to 1
)
F IGURE 5emspRepresentationoftoppriorityareaswithintheextentofsuitablehabitatofcharismaticspeciesAdecreaseinprioritycorrespondswithincreasingsizeofareasthatneedtobeprotectedForexamplethetop25priorityarearefersto25ofthesizeoftheentirelandscapeandthehighest25ofpriorityscoresfromZonationalgorithmThereforelessproportionoftop-priorityareaoverlappedwiththeextentofsuitablehabitatofthefourcharismaticmegafauna
Rep
rese
ntat
ion
()
Taxonomic diversity Phylogenetic diversity Functional diversity
020
4060
8010
0
Top5 10 17 25 5 10 17 25 5 10 17 25
CombinedTigerElephantOrangutanRhinoceros
8emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
having approximately half of tigers suitable habitat represented lessthanhalfoftheamountofpriorityareascoveredbythetigerCombiningallcharismaticspeciesimprovedtherepresentationofpriorityareasbutonlybyasmallamountcomparedtothetiger(Figure5)Wealsoidenti-fiedpriorityareasthatwerenotcoveredbyanyofthefourcharismaticspeciesrsquodistributionsegforthetop5priorityareas28(taxonomy-basedpriority)8(phylogeny-based)and18(trait-based)wereout-sidetheextentofsuitablehabitatofthecharismaticspecies
Evaluationonthepotentialoftheother180mammalspecies inSumatrainrepresentingpriorityareasrevealedthattheextentofsuit-ablehabitatwasagoodpredictorof surrogacypotential (Figure6)However species with similar size of suitable habitat representedvaryingproportionsofpriorityareasThetigerhadahighersurrogacypotentialcomparedtomostotherspecieswithsimilarsizeofsuitablehabitatTheelephantontheoppositehadanunderperformingsur-rogacypotentialthanwaspredictedbyitssizeofsuitablehabitat
4emsp |emspDISCUSSION
41emsp|emspThe role of the charismatic megafauna in Sumatra as biodiversity surrogates
We used recently developed techniques to evaluate the con-servation effectiveness of using charismatic megafauna as sur-rogates for taxonomic phylogenetic and functional diversity of
SumatranmammalsWefoundthatSumatrantigerhadthehigh-estsurrogacypotentialbecausemostof theco-occurringmam-malswerewellrepresentedwithinitsdistributionanditcoveredhigh amounts of priority areas for the three biodiversity facets(taxonomicphylogeneticandfunctionaldiversity)Thisisrelatedto its relatively large distribution compared to the other char-ismatic species in Sumatra However the tiger also had highersurrogacypotentialthanpredictedbasedonitsdistributionsizealoneThissupportsthefindingfromapreviousstudythatlargepredators have important surrogate roles for other mammals(Thorntonetal2016)
The Sumatran elephant had the second highest potential as asurrogatespecies inSumatra intermsoftherepresentationofco-occurringspeciesHoweveritcoveredalowerproportionofpriorityareasthanexpectedbyitsrangesizebecauseitdidnotoccurinmostofwesternmountainrangeswheremostofthepriorityareaswerefoundTheorangutanand rhinoceros represented relatively loweramountsoftotalpriorityareaswhichmatchedwiththeirrestricteddistributionrangeHoweveralmosttheentirerangesofthesetwospeciesencompassedtop-rankedpriorityareasThisimpliesallocat-ingconservationresourcestoprotectareaswithintherangeoftheorangutanandtherhinowouldresult inahighcontributiontotheprotectionofbroaderbiodiversitybutthisstrategyalonewilllikelybeinsufficientforSumatranbiodiversitygiventherestricteddistri-butionofthetwospecies
F IGURE 6emspTherepresentationoftop5priorityareastop10priorityareastop17priorityareasandtop25priorityareaswithinthesuitablehabitatofcharismaticmegafaunarelativetotheirextentofsuitablehabitatLettersintheplotandtheorangepointsindicatethecharismaticmegafaunaspeciesT=tigerE=AsianelephantO=SumatranorangutanR=SumatranrhinocerosGreypointsindicatetheothermammalspeciesinSumatra(180species)Bluelinesrepresentfittedvaluesofpriorityarearepresentationbasedongeneralisedadditivemodels
1 2 3 4 5
020
4060
80
Taxonomic diversity
T
OR
ETop
5
1 2 3 4 5
Phylogenetic diversity
T
OR
E
1 2 3 4 5
Functional diversity
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
10
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
17
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
25
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
Rep
rese
ntat
ion
()
log(suitable area [km sq])
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
R E FE R E N C E S
AndelmanSJampFaganWF(2000)UmbrellasandflagshipsEfficientconservation surrogates or expensivemistakesProceedings of the National Academy of Science of the United States of America97(11)5954ndash5959httpsdoiorg101073pnas100126797
BadanPusatStatistik(2012)Indonesianpopulationbasedonprovinces19711980199019952000and2010Retrievedfromwwwbpsgoid
Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
2emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
1emsp |emspINTRODUC TION
Conservingallbiodiversity featuresat thesametime isnot feasi-bledue to limited resourceshenceconservationeffortsmustbestrategically planned and prioritised (Bottrill etal 2008 JosephMaloneyampPossingham2009)Oneconservationstrategythat isoftenapplied is toemployaspeciesorgroupofspecies inmanycaseslargeandcharismaticspeciesasflagshipsAflagshipspeciesisldquoaspeciesusedasthefocusofabroaderconservationmarketingcampaign based on its possession of one ormore traits that ap-pealtothetargetaudiencerdquo(VerissimoMacMillanampSmith2011)Howevermostofthecampaignsprimarilyseekfundsdirectlyforthe flagships and are rarely aimed to benefit other biodiversity(Smith Veriacutessimo Isaac amp Jones 2012) Considering limited re-sourcesforconservationandthevastrangeofbiodiversitythatre-quireprotectionconservingflagshipspeciesintheirnaturalhabitathasagreatpotentialtocontributetothepersistenceofbiodiversitywhen properly planned
Whileflagshipspeciesdonotnecessarilyactasumbrellaspe-cieswhoseconservationconfersprotectiontoa largenumberofco-occurring species (Roberge amp Angelstam 2004)mdashcharismaticmegafaunamayserveasbothflagshipandumbrella (Caro2010)However previous work has shownmixed results as to whethercharismaticmegafaunaspeciesareeffective surrogates forbiodi-versityAndelmanandFagan(2000)reportedlittleevidencefortheeffectivenessofvarious surrogateschemes includingcharismaticspecies for regional species conservation in the United StatesSimilarlyWilliams Burgess and Rahbek (2000) found that areasidentifiedbasedonthedistributionofflagshipspeciesdonotper-form better in representing the diversity of mammals and birdsthanareas identifiedfromrandomlyselectedspecies Incontrastconservation networks for jaguarPanthera onca in LatinAmericarepresentsubstantialproportionofhigh-qualityhabitatsforotherterrestrial mammals (Thornton etal 2016) and the giant pandaAiluropoda melanoleucaisaneffectivesurrogateforendemicmam-malandbirdspeciesinChina(LiampPimm2016)InAfricathepri-ority conservation areas for theAfrican ldquoBig Fiverdquo species highlyrepresentpriorityareas for theothermammals yetprovidepoorrepresentations for amphibians reptiles invertebrates andplants(DiMininampMoilanen2014)
Mostevaluationsofsurrogatespeciesfocusedontheirrepresen-tationof taxonomicdiversityHowever taxonomicdiversity alonedoes not capture other important facets of biodiversity such asphylogeneticdiversitymdashthedistinctivenessamongspeciesbasedon
their evolutionary history (Faith 1992)mdashand functional diversitymdashthedistributionofspeciesinamultidimensionalnichespacedefinedbytheirlife-historytraits(PetcheyampGaston2006)Thislimitstheglobalunderstandingofsurrogacypotentialforcharismaticspeciesbecausedifferentfacetsofbiodiversityoftenshownon-congruentspatialpatternsForexampleglobalmammalhotspotsdefinedusingtaxonomic phylogenetic and functional diversity are not spatiallycongruent(Mazeletal2014)Similarlythereisonly46overlapamongthetoppriorityconservationareasformammalconservationacrossthethreefacets(Brumetal2017)Onacountryscalefunc-tionaldiversityofbirdsinFranceisunderrepresentedinprotectedareas whereas taxonomic diversity is overrepresented (Devictoretal2010)
SumatraisapartoftheSundalandbiodiversityhotspotwheretheuseof charismaticmegafauna to guide conservationeffortsis a common practice (Ministry of Forestry of the Republic ofIndonesia2007PHKA2015SoehartonoSusiloAndayanietal2007 Soehartono Susilo Sitompul etal 2007 SoehartonoWibisonoetal2007)TheprotectedareacoverageofSumatrarequiresanexpansionfromthecurrent~11ndash17toachievethecommitmentssetundertheConventiononBiologicalDiversitysAichi Target 11 assuming proportional allocation to land areaacross the major islands in Indonesia Conservation efforts inSumatra have been largely targeted towards four charismaticmegafauna species the Sumatran tigerPanthera tigris sumatraetheSumatranelephantElephas maximus sumatranustheSumatranorangutanPongo abeliiandtheSumatranrhinocerosDicerorhinus sumatrensis Conservationists often propose that these largemammalshaveanumbrellaeffectandthatsavingthemwillalsosaveanumberofotherco-occurringspeciesHoweverthispro-claimedumbrellaeffectremainslargelyuntestedespeciallywhenitcomestomultiplefacetsofbiodiversitysuchasfunctionalandphylogeneticdiversityInthisworkweaddressedthisimportantshortfallandevaluatedwhethertheavailablehabitatforfourflag-shipspeciesinSumatraisrepresentativeofthetaxonomicfunc-tional and phylogeneticmammal diversity (hereafter ldquosurrogacypotentialrdquo)
Our firstaimwas tomeasure thehabitatoverlapbetweenthefourcharismaticspeciesofSumatraandtheothernativeterrestrialmammalspeciesontheislandThesecondaimwastoidentifythepriority areas formammal conservation in Sumatra based on tax-onomic phylogenetic and functional diversity and to assess howmuch these areas would benefit from the protection of the fourcharismaticspecies
K E Y W O R D S
functionaldiversityphylogeneticdiversityspatialconservationprioritisationSumatranelephantSumatranorangutanSumatranrhinocerosSumatrantigersurrogatespecies
emspensp emsp | emsp3Journal of Applied EcologySIBARANI et Al
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy region
Sumatra isoneofthe largest islands in Indonesiawithatotalareaof430000km2 (GADM2009)The island is surroundedbymanysmallersatelliteislandsyetthisstudyfocusedonlyonthemainis-land (Figure1) Forest landuse zones aredivided into three func-tionsbiodiversityconservation(106oftheisland)watersystemprotection (13) and production (356)Other land uses (408of the island) include agriculture land and settlements (MargonoTurubanova Zhuravleva Potapov amp Tyukavina 2012) Between1990 and 2010 an estimated 75million hectares of primary for-estinSumatrawereclearedand23millionhectareshavebeende-graded leavingonly30ofSumatracoveredbyprimaryforest in2010 (Margonoetal 2012)ThehumanpopulationofSumatra in2010was506millionwithagrowthrateof145between2000and2010(BadanPusatStatistik2012)
22emsp|emspMammal distribution data
We obtained the list of native terrestrial mammal species inSumatrausing(a)thesearchtoolonIUCNRedListofThreatenedSpecieswebsite(wwwiucnredlistorg)and(b)theIUCNgeographicdistributionrangesforterrestrialmammals(IUCN2016)Becausethetwolistsdidnotreturnthesamenumberofspecieswemerged
themandcheckedthespeciesinformationpagesontheIUCNRedListwebsitetofilterspeciesthatoccurinSumatra(excludingspe-ciesthatonlyoccuronsatelliteislands)Thisresultedin193mam-malspeciesbeinglisted includingthefoursurrogatespecies(seeAppendixS1)
Giventhe lackofcomprehensiveoccurrencedata fordevelop-ingstatisticaldistributionmodelsforallspeciesweuseddeductive(expert-driven)habitatsuitabilitymodels to representspeciesrsquodis-tributions on the island (Rondinini etal 2011) Habitat suitabilitymodelshavebeenusedinanumberofotherstudiesonaregional(egThorntonetal2016)andglobalscale(egBrumetal2017)wherecomprehensiveoccurrencedatawereunavailableRondininietal(2011)assessedspeciesrsquohabitatsuitabilitybyconsideringspe-cieshabitatpreferencesforthreeenvironmentalvariablesthetypesoflandcoverelevationrangeandhydrologicalfeaturesTheresult-ingdeductivemodelsconsistof threeclassesofhabitatsuitability(Rondininietal2011)
i Highhabitat suitability representing theprimaryhabitatwherethespeciescanpersist
iiMediumhabitatsuitabilityrepresentingsecondaryhabitatwherethespeciescanbefoundyetcannotpersistwithouttheprimaryhabitatand
iiiLowhabitatsuitabilityrepresentingareaswherethespeciesaregenerallynotfoundorunlikelytooccur
F IGURE 1emspMapofthestudyregionSumatraIslandSmallinsertmapshowsthelocationoftheislandinIndonesia
4emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
In the spatial prioritisation analysis we only used areas of highhabitat suitability to represent theoccurrenceof the species (here-after ldquoextent of suitable habitatrdquo) becausewe intendedwanted theresulting conservation area systems to include areaswhere speciesaremost likelytopersistOfthe193nativeterrestrialmammalspe-cies inSumatra thetworecentlysplitorangutanpopulations (Nateretal2017)wereconsideredasonespeciesandeightspecieswerenotmodelledbyRondininietal(2011)thereforeouranalysisincludedatotalof184species(includingthefourcharismaticspecies)
23emsp|emspAssessing the representation of mammal species by the charismatic megafauna
Weassessedthesurrogacypotentialofcharismaticmegafaunaspe-cies by overlaying their extent of suitable habitatwith that of allothermammals Representationwas calculated as the proportionof a speciesrsquo extent of suitable habitat overlappingwith thehabi-tatofeachcharismaticmegafaunaspeciesWeperformedall spa-tialdataprocessingusing therpackages ldquosprdquo (PebesmaampBivand2005)andldquorasterrdquo(HijmansampvanEtten2012)inrversion341(RDevelopmentCoreTeam2008)
24emsp|emspAssessing the representation of priority areas based on multiple facets of biodiversity
We identified conservation priority areas using the Zonation v4software(Moilanenetal2014)TheinputdataforZonationanaly-sisarerastermapsofbiodiversityfeatures(egspeciesandhabitattypes)whichrepresenttheirspatialdistributionTheZonationalgo-rithmstarts from the full extentof the landscapeof interest andtheniterativelyremovesareaswiththelowestvalueforconserva-tionbasedontheoccurrencelevelofbiodiversityfeatures(Moilanenetal2005)Thisiterativeremovalprocessgeneratesamapshow-ing a hierarchic ranking of conservation priorities throughout thelandscape(MoilanenKujalaampLeathwick2009)Eachrastercelloftheoutputmap contains a rankof conservationpriorities rangingbetween0(lowestpriority)and1(highestpriority)thatcanbevisu-alisedasahierarchicalzonedmapoftoppriorityareasforconserva-tionZonationhasalreadybeenusedforassessingumbrellaeffectsofsurrogatespecies(DiMininampMoilanen2014)andexaminingcon-gruencyofpriority areas formultiple facetsofbiodiversity (Brumetal2017PollockThuillerampJetz2017StreckerOldenWhittierampPaukert2011)
We used Core Area Zonation as the cell removal rules inZonationwhichranksthecellsacrossthe landscapebasedonthemost importantoccurrenceof a feature andhencecould identifycore areas of features in biodiversity-poor areas (Moilanen etal2014)We also incorporated connectivity considerations by usingthe Boundary Length Penalty to produce more compact reservesolutions (MoilanenampWintle2007)We ran three separate anal-yses to identify priorities for threedifferent biodiversity facets aspecies-level analysis (taxonomic prioritisation) an analysis basedonphylogeneticgroups(phylogeneticprioritisation)andananalysis
basedonfunctionalgroups(functionalprioritisation)Furthertech-nicaldetailsareprovidedinAppendixS2
25emsp|emspBiodiversity features for spatial prioritisation
Weusedindividualspeciesasthebiodiversityfeaturesforthespa-tialprioritisationbasedontaxonomicdiversityWeperformedarea-weighted resampling to scaleup thehabitat suitabilitymaps fromtheoriginal300mresolutionto1kmWeusedaresolutionof1kmas a compromise between computational time and relevance forconservationmanagement on the islandWeweighted14 speciesendemictoSumatratwiceasmuchasthenon-endemicspeciestorepresentthehigherglobalvalueoftheirconservationontheislandWealsoperformedasensitivityanalysisonalternativeweightingofendemicspeciesbuttheresultsshowednosubstantialdifferences(seeAppendixS4)
For spatial prioritisation based on phylogenetic diversity wedefined phylogenetic groups following the framework developedbyStreckeretal(2011)andBrumetal(2017)Weusedthemam-malian phylogenetic supertree created by Bininda-Emonds etal(2007)andupdatedbyFritzBininda-EmondsandPurvis(2009)tocreateaphylogeneticdistancematrixamong181mammalspeciesinSumatraafterexcludingthreespecieswhichwerenotavailablein themammaliansupertreeWethenperformedprincipalcoordi-nateanalysisonthephylogeneticdistancematrixandselectedthefirst16eigenvectorswhichexplainedgt1oftotalvariationTheseeigenvectors altogether accounted for 69 of the total variationEacheigenvectorwassplitinto10quantiles(seeAppendixS4forthesensitivitytest)andthenconverted intobinaryvariablesOurquantileswerewiderthanthoseusedinBrumetal(2017)becausewe had fewer number of species in Sumatra To represent phylo-geneticgroups inspatialmapswecreatedabinarymatrixofspe-ciestimesphylogeneticgroupArea-weightedhabitatsuitabilitymapsat1kmresolutionwerereclassifiedintobinarymapswithathresholdof005 (this threshold reduces the riskof introducingcommissionerrorswithoutpenalisingspecieswithnarrowhabitatdistributions)andthenwereconvertedintogridtimesspeciesmatrixFinallywemul-tipliedthetwomatricestoobtaingridtimesphylogeneticgroupsmatrixinwhichagridcellcontainedthenumberofspeciesbelongingtoaparticularphylogenetic groupWe thengenerated spatialmapsofphylogeneticgroupdistributionfromthismatrix
Wemappedmammalianfunctionaltraitswithsimilarprocedurewithphylogeny-basedprioritisationusing life-history traitsasop-posed to phylogenetic eigenvectorsWe selected five life-historyand ecological categories represented by nine traits adult bodymassmaximumlongevityreproductivespeed(weaningagegesta-tionlength)reproductionoutput(neonatebodymasslittersizeandlittersperyear)andresourceuse(trophiclevelandhabitatbreadth)WeusedtheglobaldatasetforterrestrialmammaltraitscompiledbyPacificietal (2013)andDiMarcoandSantini (2015)fromvarioussourcessuchasPanTHERIA(Jonesetal2009)andAnAge(Tacutuetal2013)Weassignedthepresenceabsenceofeachlevelofcate-goricaltraitsinabinarymatrixofspeciestimestraitWesplitcontinuous
emspensp emsp | emsp5Journal of Applied EcologySIBARANI et Al
traitsinto10quantilesandweassignedpresenceabsenceofeachsame-sizetraitleveltospeciesNextwemultipliedthegridtimesspe-ciesmatrixwithspeciestimestraitmatrixWeconvertedtheresultingmatrixofgridtimestraitintospatialmapsoffunctionaltraitlevelsThedetailedprocedureofdatapreparationisprovidedinAppendixS2
Werantheprioritisationanalysisseparatelyusingspeciesrsquohabi-tatsuitabilitymapsasinputsintaxonomy-basedprioritisationphy-logeneticgroupmapsinphylogeny-basedprioritisationandlevelsoffunctionaltraitsintrait-basedprioritisationWethenextractedthe
top51017and25ofpriorityareasforeachprioritisationscenariosandoverlaid themwith theextentof suitablehabitatofthecharismaticmegafaunaspeciesWemeasuredthesurrogacypo-tentialofcharismaticmegafaunaastheproportionofpriorityareasacrossSumatrathatoverlappedwiththeextentofsuitablehabitatofthespeciesunderconsiderationInadditionwealsocalculatedthesurrogacypotentialsofothermammal species inSumatra tocom-pare the performance of the four charismatic megafauna specieswiththatofotherspecies
F IGURE 2emspTherepresentationoftheco-occurringmammalspecieswithinthesuitablehabitatofcharismaticmegafauna(a)overalland(b)categorisedaccordingtotheirIUCNRedListcategoriesDDDataDeficientLCLeastConcernNTNearThreatenedVUVulnerableENEndangeredCRCriticallyEndangeredNotethatthescalesofy-axisof(b)aredifferentacrossthefourcharismaticmegafaunaspecies
TigerE
lephantO
rangutanR
hinoceros
0 25 50 75 100
0
50
100
150
0
50
100
150
0
50
100
150
0
50
100
150
Representation ()
Num
ber o
f spe
cies
Tiger Elephant Orangutan Rhinoceros
0 25 50 75 100 0 25 50 75 0 20 40 60 80 0 3 6 9
DD (N = 13)
LC (N = 110)
NT (N = 20)
VU (N = 26)
EN (N = 12)
CR (N = 3)
Representation ()
IUC
N R
ed L
ist c
ateg
orie
s
(a)
(b)
6emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
3emsp |emspRESULTS
31emsp|emspSurrogacy for terrestrial mammal species
Among the four charismaticmegafauna species the tiger had thehighest spatial overlap with other mammal species represent-ingameanof52 (SD=27)of theextentof suitablehabitatofother Sumatranmammals (Figure2) The representation levels forothercharismatic speciesweremuch lower18 for theelephant(SD=12) 9 for the orangutan (SD=11) and 2 for the rhi-noceros(SD=2)Onlytwospecieshadahighspatialoverlapwiththeelephant(ie93forthelesserlarge-footedmyotisMyotis has-seltii and85 for thebig-earedhorseshoebatRhinolophus macro-tis)Likewiseonly twospecieshadahighspatialoverlapwith theorangutan(ie81forthebig-earedhorseshoebatand71forthepen-tailedtreeshrewPtilocercus lowii)
Mostofthesuitablehabitatfororangutanandrhinocerosover-lappedwiththetigerbutonly41oftheelephantsextentofsuit-ablehabitatoverlappedwiththetigersThesuitablehabitatfortigeroverlappedsubstantially(52)withthecriticallyendangeredSundapangolin Manis javanica Of the 12 endangered species (Figure2)onlyonewasunderrepresentedbythetigeriethehairy-nosedotter
Lutra sumatranawithrepresentationlevelof12Theother11en-dangeredspecieswerewellrepresentedbythetigerwiththeover-laprangingfrom40to89Combiningthefoursurrogatespeciesonlyimprovedtherepresentationlevelsbyameanof5(SD=6range=0ndash12)comparedtotheperformanceofthetigeralone
32emsp|emspSurrogacy for priority areas based on multiple facets of biodiversity
Wediscoveredsubstantialspatialmismatchesamongtheareasiden-tifiedundertaxonomicphylogeneticandfunctionaldiversityprior-itisation scenarios (Figure3)When looking at the top5priorityareasforeachbiodiversityfacetswhichaltogetherencompassedanareaof21595km2we foundanoverlapofonly3227km2 (15)acrossthethreefacetsPriorityareassharedamongthethreeprior-itisationscenariosmostlyoccurredinhighlandsofnorthernSumatraandwesternmountainrangesIntaxonomy-basedprioritisationthepriorityareasweremorespreadoutacrosstheislandincludingcen-tral lowlandandeasterncoastsThespatial solution forprioritisa-tionbasedonphylogeneticgroupswasmoreclumpedinthewesternhalfoftheislandPriorityareasforconservingfunctionaltraitswere
F IGURE 3emspPriorityconservationareasinSumatrabasedonmultiplefacetsofbiodiversityThetopmapsreportthespatialprioritisationresultsreportingtherankingofconservationprioritythroughoutthelandscape(with0meaninglowestimportanceand1meaninghighestimportance)WecategorisedhighpriorityareasintofourgroupsofnestedpriorityrankingsTop5(valuesofgt095)top10(gt090)top17(gt083)andtop25(gt075)Theinsetmapsreportthespatialdistributionofcharismaticmegafaunaspecies
Priority rankingTop 5Top 10Top 17Top 25
Taxonomic diversity Phylogenetic diversity Functional diversity
Maps of charismaticmegafauna species
Tiger Elephant Orangutan Rhinoceros
0 400200 km
Extent of suitable habitat
emspensp emsp | emsp7Journal of Applied EcologySIBARANI et Al
morecongruenttophylogeny-based(20overlap)thantaxonomy-basedprioritisation(17overlap)
Ingeneralmostoftheextentofsuitablehabitatofthecharis-maticspecieswasofhighconservationpriority(Figure4)Theorang-utanandrhinoceroscoveredareasinSumatrawithrelativelyhigherconservationpriorityranksthanthetigerandelephantAmongthefour elephant had the most variability in representing conserva-tionprioritiesegfortaxonomicprioritisationIQRelephant=044
IQRtiger=023 IQRorangutan=010 IQRrhinoceros=005 (com-pletesummarystatisticsinAppendixS4)
Whilemostofthesuitablehabitatsfortheorangutanandrhinoc-erosoverlappedwithareasofhighconservationprioritytheseonlyac-countedforsmallproportionoftoppriorityareasgiventherestricteddistributionofthesespecies(Figure5)Thetigerssuitablehabitathadthehighestarealcoverageofpriorityareasforthethreebiodiversityfac-etsanditrepresentedphylogeneticprioritiesparticularlywellElephant
F IGURE 4emspBoxplotsshowingthevariationofconservationpriorityrankswithintheextentofsuitablehabitatofcharismaticmegafaunaspecies The y-axisrepresentstheconservationpriorityranksthatwerecomputedbasedoniterativecellremovalprocessofZonationrangingfrom0(lowestpriority)to1(highestpriority)
Taxonomic diversity Phylogenetic diversity Functional diversity
Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino
000
025
050
075
100
Charismatic megafauna
Con
serv
atio
n pr
iorit
y (0
to 1
)
F IGURE 5emspRepresentationoftoppriorityareaswithintheextentofsuitablehabitatofcharismaticspeciesAdecreaseinprioritycorrespondswithincreasingsizeofareasthatneedtobeprotectedForexamplethetop25priorityarearefersto25ofthesizeoftheentirelandscapeandthehighest25ofpriorityscoresfromZonationalgorithmThereforelessproportionoftop-priorityareaoverlappedwiththeextentofsuitablehabitatofthefourcharismaticmegafauna
Rep
rese
ntat
ion
()
Taxonomic diversity Phylogenetic diversity Functional diversity
020
4060
8010
0
Top5 10 17 25 5 10 17 25 5 10 17 25
CombinedTigerElephantOrangutanRhinoceros
8emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
having approximately half of tigers suitable habitat represented lessthanhalfoftheamountofpriorityareascoveredbythetigerCombiningallcharismaticspeciesimprovedtherepresentationofpriorityareasbutonlybyasmallamountcomparedtothetiger(Figure5)Wealsoidenti-fiedpriorityareasthatwerenotcoveredbyanyofthefourcharismaticspeciesrsquodistributionsegforthetop5priorityareas28(taxonomy-basedpriority)8(phylogeny-based)and18(trait-based)wereout-sidetheextentofsuitablehabitatofthecharismaticspecies
Evaluationonthepotentialoftheother180mammalspecies inSumatrainrepresentingpriorityareasrevealedthattheextentofsuit-ablehabitatwasagoodpredictorof surrogacypotential (Figure6)However species with similar size of suitable habitat representedvaryingproportionsofpriorityareasThetigerhadahighersurrogacypotentialcomparedtomostotherspecieswithsimilarsizeofsuitablehabitatTheelephantontheoppositehadanunderperformingsur-rogacypotentialthanwaspredictedbyitssizeofsuitablehabitat
4emsp |emspDISCUSSION
41emsp|emspThe role of the charismatic megafauna in Sumatra as biodiversity surrogates
We used recently developed techniques to evaluate the con-servation effectiveness of using charismatic megafauna as sur-rogates for taxonomic phylogenetic and functional diversity of
SumatranmammalsWefoundthatSumatrantigerhadthehigh-estsurrogacypotentialbecausemostof theco-occurringmam-malswerewellrepresentedwithinitsdistributionanditcoveredhigh amounts of priority areas for the three biodiversity facets(taxonomicphylogeneticandfunctionaldiversity)Thisisrelatedto its relatively large distribution compared to the other char-ismatic species in Sumatra However the tiger also had highersurrogacypotentialthanpredictedbasedonitsdistributionsizealoneThissupportsthefindingfromapreviousstudythatlargepredators have important surrogate roles for other mammals(Thorntonetal2016)
The Sumatran elephant had the second highest potential as asurrogatespecies inSumatra intermsoftherepresentationofco-occurringspeciesHoweveritcoveredalowerproportionofpriorityareasthanexpectedbyitsrangesizebecauseitdidnotoccurinmostofwesternmountainrangeswheremostofthepriorityareaswerefoundTheorangutanand rhinoceros represented relatively loweramountsoftotalpriorityareaswhichmatchedwiththeirrestricteddistributionrangeHoweveralmosttheentirerangesofthesetwospeciesencompassedtop-rankedpriorityareasThisimpliesallocat-ingconservationresourcestoprotectareaswithintherangeoftheorangutanandtherhinowouldresult inahighcontributiontotheprotectionofbroaderbiodiversitybutthisstrategyalonewilllikelybeinsufficientforSumatranbiodiversitygiventherestricteddistri-butionofthetwospecies
F IGURE 6emspTherepresentationoftop5priorityareastop10priorityareastop17priorityareasandtop25priorityareaswithinthesuitablehabitatofcharismaticmegafaunarelativetotheirextentofsuitablehabitatLettersintheplotandtheorangepointsindicatethecharismaticmegafaunaspeciesT=tigerE=AsianelephantO=SumatranorangutanR=SumatranrhinocerosGreypointsindicatetheothermammalspeciesinSumatra(180species)Bluelinesrepresentfittedvaluesofpriorityarearepresentationbasedongeneralisedadditivemodels
1 2 3 4 5
020
4060
80
Taxonomic diversity
T
OR
ETop
5
1 2 3 4 5
Phylogenetic diversity
T
OR
E
1 2 3 4 5
Functional diversity
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
10
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
17
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
25
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
Rep
rese
ntat
ion
()
log(suitable area [km sq])
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
R E FE R E N C E S
AndelmanSJampFaganWF(2000)UmbrellasandflagshipsEfficientconservation surrogates or expensivemistakesProceedings of the National Academy of Science of the United States of America97(11)5954ndash5959httpsdoiorg101073pnas100126797
BadanPusatStatistik(2012)Indonesianpopulationbasedonprovinces19711980199019952000and2010Retrievedfromwwwbpsgoid
Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
emspensp emsp | emsp3Journal of Applied EcologySIBARANI et Al
2emsp |emspMATERIAL S AND METHODS
21emsp|emspStudy region
Sumatra isoneofthe largest islands in Indonesiawithatotalareaof430000km2 (GADM2009)The island is surroundedbymanysmallersatelliteislandsyetthisstudyfocusedonlyonthemainis-land (Figure1) Forest landuse zones aredivided into three func-tionsbiodiversityconservation(106oftheisland)watersystemprotection (13) and production (356)Other land uses (408of the island) include agriculture land and settlements (MargonoTurubanova Zhuravleva Potapov amp Tyukavina 2012) Between1990 and 2010 an estimated 75million hectares of primary for-estinSumatrawereclearedand23millionhectareshavebeende-graded leavingonly30ofSumatracoveredbyprimaryforest in2010 (Margonoetal 2012)ThehumanpopulationofSumatra in2010was506millionwithagrowthrateof145between2000and2010(BadanPusatStatistik2012)
22emsp|emspMammal distribution data
We obtained the list of native terrestrial mammal species inSumatrausing(a)thesearchtoolonIUCNRedListofThreatenedSpecieswebsite(wwwiucnredlistorg)and(b)theIUCNgeographicdistributionrangesforterrestrialmammals(IUCN2016)Becausethetwolistsdidnotreturnthesamenumberofspecieswemerged
themandcheckedthespeciesinformationpagesontheIUCNRedListwebsitetofilterspeciesthatoccurinSumatra(excludingspe-ciesthatonlyoccuronsatelliteislands)Thisresultedin193mam-malspeciesbeinglisted includingthefoursurrogatespecies(seeAppendixS1)
Giventhe lackofcomprehensiveoccurrencedata fordevelop-ingstatisticaldistributionmodelsforallspeciesweuseddeductive(expert-driven)habitatsuitabilitymodels to representspeciesrsquodis-tributions on the island (Rondinini etal 2011) Habitat suitabilitymodelshavebeenusedinanumberofotherstudiesonaregional(egThorntonetal2016)andglobalscale(egBrumetal2017)wherecomprehensiveoccurrencedatawereunavailableRondininietal(2011)assessedspeciesrsquohabitatsuitabilitybyconsideringspe-cieshabitatpreferencesforthreeenvironmentalvariablesthetypesoflandcoverelevationrangeandhydrologicalfeaturesTheresult-ingdeductivemodelsconsistof threeclassesofhabitatsuitability(Rondininietal2011)
i Highhabitat suitability representing theprimaryhabitatwherethespeciescanpersist
iiMediumhabitatsuitabilityrepresentingsecondaryhabitatwherethespeciescanbefoundyetcannotpersistwithouttheprimaryhabitatand
iiiLowhabitatsuitabilityrepresentingareaswherethespeciesaregenerallynotfoundorunlikelytooccur
F IGURE 1emspMapofthestudyregionSumatraIslandSmallinsertmapshowsthelocationoftheislandinIndonesia
4emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
In the spatial prioritisation analysis we only used areas of highhabitat suitability to represent theoccurrenceof the species (here-after ldquoextent of suitable habitatrdquo) becausewe intendedwanted theresulting conservation area systems to include areaswhere speciesaremost likelytopersistOfthe193nativeterrestrialmammalspe-cies inSumatra thetworecentlysplitorangutanpopulations (Nateretal2017)wereconsideredasonespeciesandeightspecieswerenotmodelledbyRondininietal(2011)thereforeouranalysisincludedatotalof184species(includingthefourcharismaticspecies)
23emsp|emspAssessing the representation of mammal species by the charismatic megafauna
Weassessedthesurrogacypotentialofcharismaticmegafaunaspe-cies by overlaying their extent of suitable habitatwith that of allothermammals Representationwas calculated as the proportionof a speciesrsquo extent of suitable habitat overlappingwith thehabi-tatofeachcharismaticmegafaunaspeciesWeperformedall spa-tialdataprocessingusing therpackages ldquosprdquo (PebesmaampBivand2005)andldquorasterrdquo(HijmansampvanEtten2012)inrversion341(RDevelopmentCoreTeam2008)
24emsp|emspAssessing the representation of priority areas based on multiple facets of biodiversity
We identified conservation priority areas using the Zonation v4software(Moilanenetal2014)TheinputdataforZonationanaly-sisarerastermapsofbiodiversityfeatures(egspeciesandhabitattypes)whichrepresenttheirspatialdistributionTheZonationalgo-rithmstarts from the full extentof the landscapeof interest andtheniterativelyremovesareaswiththelowestvalueforconserva-tionbasedontheoccurrencelevelofbiodiversityfeatures(Moilanenetal2005)Thisiterativeremovalprocessgeneratesamapshow-ing a hierarchic ranking of conservation priorities throughout thelandscape(MoilanenKujalaampLeathwick2009)Eachrastercelloftheoutputmap contains a rankof conservationpriorities rangingbetween0(lowestpriority)and1(highestpriority)thatcanbevisu-alisedasahierarchicalzonedmapoftoppriorityareasforconserva-tionZonationhasalreadybeenusedforassessingumbrellaeffectsofsurrogatespecies(DiMininampMoilanen2014)andexaminingcon-gruencyofpriority areas formultiple facetsofbiodiversity (Brumetal2017PollockThuillerampJetz2017StreckerOldenWhittierampPaukert2011)
We used Core Area Zonation as the cell removal rules inZonationwhichranksthecellsacrossthe landscapebasedonthemost importantoccurrenceof a feature andhencecould identifycore areas of features in biodiversity-poor areas (Moilanen etal2014)We also incorporated connectivity considerations by usingthe Boundary Length Penalty to produce more compact reservesolutions (MoilanenampWintle2007)We ran three separate anal-yses to identify priorities for threedifferent biodiversity facets aspecies-level analysis (taxonomic prioritisation) an analysis basedonphylogeneticgroups(phylogeneticprioritisation)andananalysis
basedonfunctionalgroups(functionalprioritisation)Furthertech-nicaldetailsareprovidedinAppendixS2
25emsp|emspBiodiversity features for spatial prioritisation
Weusedindividualspeciesasthebiodiversityfeaturesforthespa-tialprioritisationbasedontaxonomicdiversityWeperformedarea-weighted resampling to scaleup thehabitat suitabilitymaps fromtheoriginal300mresolutionto1kmWeusedaresolutionof1kmas a compromise between computational time and relevance forconservationmanagement on the islandWeweighted14 speciesendemictoSumatratwiceasmuchasthenon-endemicspeciestorepresentthehigherglobalvalueoftheirconservationontheislandWealsoperformedasensitivityanalysisonalternativeweightingofendemicspeciesbuttheresultsshowednosubstantialdifferences(seeAppendixS4)
For spatial prioritisation based on phylogenetic diversity wedefined phylogenetic groups following the framework developedbyStreckeretal(2011)andBrumetal(2017)Weusedthemam-malian phylogenetic supertree created by Bininda-Emonds etal(2007)andupdatedbyFritzBininda-EmondsandPurvis(2009)tocreateaphylogeneticdistancematrixamong181mammalspeciesinSumatraafterexcludingthreespecieswhichwerenotavailablein themammaliansupertreeWethenperformedprincipalcoordi-nateanalysisonthephylogeneticdistancematrixandselectedthefirst16eigenvectorswhichexplainedgt1oftotalvariationTheseeigenvectors altogether accounted for 69 of the total variationEacheigenvectorwassplitinto10quantiles(seeAppendixS4forthesensitivitytest)andthenconverted intobinaryvariablesOurquantileswerewiderthanthoseusedinBrumetal(2017)becausewe had fewer number of species in Sumatra To represent phylo-geneticgroups inspatialmapswecreatedabinarymatrixofspe-ciestimesphylogeneticgroupArea-weightedhabitatsuitabilitymapsat1kmresolutionwerereclassifiedintobinarymapswithathresholdof005 (this threshold reduces the riskof introducingcommissionerrorswithoutpenalisingspecieswithnarrowhabitatdistributions)andthenwereconvertedintogridtimesspeciesmatrixFinallywemul-tipliedthetwomatricestoobtaingridtimesphylogeneticgroupsmatrixinwhichagridcellcontainedthenumberofspeciesbelongingtoaparticularphylogenetic groupWe thengenerated spatialmapsofphylogeneticgroupdistributionfromthismatrix
Wemappedmammalianfunctionaltraitswithsimilarprocedurewithphylogeny-basedprioritisationusing life-history traitsasop-posed to phylogenetic eigenvectorsWe selected five life-historyand ecological categories represented by nine traits adult bodymassmaximumlongevityreproductivespeed(weaningagegesta-tionlength)reproductionoutput(neonatebodymasslittersizeandlittersperyear)andresourceuse(trophiclevelandhabitatbreadth)WeusedtheglobaldatasetforterrestrialmammaltraitscompiledbyPacificietal (2013)andDiMarcoandSantini (2015)fromvarioussourcessuchasPanTHERIA(Jonesetal2009)andAnAge(Tacutuetal2013)Weassignedthepresenceabsenceofeachlevelofcate-goricaltraitsinabinarymatrixofspeciestimestraitWesplitcontinuous
emspensp emsp | emsp5Journal of Applied EcologySIBARANI et Al
traitsinto10quantilesandweassignedpresenceabsenceofeachsame-sizetraitleveltospeciesNextwemultipliedthegridtimesspe-ciesmatrixwithspeciestimestraitmatrixWeconvertedtheresultingmatrixofgridtimestraitintospatialmapsoffunctionaltraitlevelsThedetailedprocedureofdatapreparationisprovidedinAppendixS2
Werantheprioritisationanalysisseparatelyusingspeciesrsquohabi-tatsuitabilitymapsasinputsintaxonomy-basedprioritisationphy-logeneticgroupmapsinphylogeny-basedprioritisationandlevelsoffunctionaltraitsintrait-basedprioritisationWethenextractedthe
top51017and25ofpriorityareasforeachprioritisationscenariosandoverlaid themwith theextentof suitablehabitatofthecharismaticmegafaunaspeciesWemeasuredthesurrogacypo-tentialofcharismaticmegafaunaastheproportionofpriorityareasacrossSumatrathatoverlappedwiththeextentofsuitablehabitatofthespeciesunderconsiderationInadditionwealsocalculatedthesurrogacypotentialsofothermammal species inSumatra tocom-pare the performance of the four charismatic megafauna specieswiththatofotherspecies
F IGURE 2emspTherepresentationoftheco-occurringmammalspecieswithinthesuitablehabitatofcharismaticmegafauna(a)overalland(b)categorisedaccordingtotheirIUCNRedListcategoriesDDDataDeficientLCLeastConcernNTNearThreatenedVUVulnerableENEndangeredCRCriticallyEndangeredNotethatthescalesofy-axisof(b)aredifferentacrossthefourcharismaticmegafaunaspecies
TigerE
lephantO
rangutanR
hinoceros
0 25 50 75 100
0
50
100
150
0
50
100
150
0
50
100
150
0
50
100
150
Representation ()
Num
ber o
f spe
cies
Tiger Elephant Orangutan Rhinoceros
0 25 50 75 100 0 25 50 75 0 20 40 60 80 0 3 6 9
DD (N = 13)
LC (N = 110)
NT (N = 20)
VU (N = 26)
EN (N = 12)
CR (N = 3)
Representation ()
IUC
N R
ed L
ist c
ateg
orie
s
(a)
(b)
6emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
3emsp |emspRESULTS
31emsp|emspSurrogacy for terrestrial mammal species
Among the four charismaticmegafauna species the tiger had thehighest spatial overlap with other mammal species represent-ingameanof52 (SD=27)of theextentof suitablehabitatofother Sumatranmammals (Figure2) The representation levels forothercharismatic speciesweremuch lower18 for theelephant(SD=12) 9 for the orangutan (SD=11) and 2 for the rhi-noceros(SD=2)Onlytwospecieshadahighspatialoverlapwiththeelephant(ie93forthelesserlarge-footedmyotisMyotis has-seltii and85 for thebig-earedhorseshoebatRhinolophus macro-tis)Likewiseonly twospecieshadahighspatialoverlapwith theorangutan(ie81forthebig-earedhorseshoebatand71forthepen-tailedtreeshrewPtilocercus lowii)
Mostofthesuitablehabitatfororangutanandrhinocerosover-lappedwiththetigerbutonly41oftheelephantsextentofsuit-ablehabitatoverlappedwiththetigersThesuitablehabitatfortigeroverlappedsubstantially(52)withthecriticallyendangeredSundapangolin Manis javanica Of the 12 endangered species (Figure2)onlyonewasunderrepresentedbythetigeriethehairy-nosedotter
Lutra sumatranawithrepresentationlevelof12Theother11en-dangeredspecieswerewellrepresentedbythetigerwiththeover-laprangingfrom40to89Combiningthefoursurrogatespeciesonlyimprovedtherepresentationlevelsbyameanof5(SD=6range=0ndash12)comparedtotheperformanceofthetigeralone
32emsp|emspSurrogacy for priority areas based on multiple facets of biodiversity
Wediscoveredsubstantialspatialmismatchesamongtheareasiden-tifiedundertaxonomicphylogeneticandfunctionaldiversityprior-itisation scenarios (Figure3)When looking at the top5priorityareasforeachbiodiversityfacetswhichaltogetherencompassedanareaof21595km2we foundanoverlapofonly3227km2 (15)acrossthethreefacetsPriorityareassharedamongthethreeprior-itisationscenariosmostlyoccurredinhighlandsofnorthernSumatraandwesternmountainrangesIntaxonomy-basedprioritisationthepriorityareasweremorespreadoutacrosstheislandincludingcen-tral lowlandandeasterncoastsThespatial solution forprioritisa-tionbasedonphylogeneticgroupswasmoreclumpedinthewesternhalfoftheislandPriorityareasforconservingfunctionaltraitswere
F IGURE 3emspPriorityconservationareasinSumatrabasedonmultiplefacetsofbiodiversityThetopmapsreportthespatialprioritisationresultsreportingtherankingofconservationprioritythroughoutthelandscape(with0meaninglowestimportanceand1meaninghighestimportance)WecategorisedhighpriorityareasintofourgroupsofnestedpriorityrankingsTop5(valuesofgt095)top10(gt090)top17(gt083)andtop25(gt075)Theinsetmapsreportthespatialdistributionofcharismaticmegafaunaspecies
Priority rankingTop 5Top 10Top 17Top 25
Taxonomic diversity Phylogenetic diversity Functional diversity
Maps of charismaticmegafauna species
Tiger Elephant Orangutan Rhinoceros
0 400200 km
Extent of suitable habitat
emspensp emsp | emsp7Journal of Applied EcologySIBARANI et Al
morecongruenttophylogeny-based(20overlap)thantaxonomy-basedprioritisation(17overlap)
Ingeneralmostoftheextentofsuitablehabitatofthecharis-maticspecieswasofhighconservationpriority(Figure4)Theorang-utanandrhinoceroscoveredareasinSumatrawithrelativelyhigherconservationpriorityranksthanthetigerandelephantAmongthefour elephant had the most variability in representing conserva-tionprioritiesegfortaxonomicprioritisationIQRelephant=044
IQRtiger=023 IQRorangutan=010 IQRrhinoceros=005 (com-pletesummarystatisticsinAppendixS4)
Whilemostofthesuitablehabitatsfortheorangutanandrhinoc-erosoverlappedwithareasofhighconservationprioritytheseonlyac-countedforsmallproportionoftoppriorityareasgiventherestricteddistributionofthesespecies(Figure5)Thetigerssuitablehabitathadthehighestarealcoverageofpriorityareasforthethreebiodiversityfac-etsanditrepresentedphylogeneticprioritiesparticularlywellElephant
F IGURE 4emspBoxplotsshowingthevariationofconservationpriorityrankswithintheextentofsuitablehabitatofcharismaticmegafaunaspecies The y-axisrepresentstheconservationpriorityranksthatwerecomputedbasedoniterativecellremovalprocessofZonationrangingfrom0(lowestpriority)to1(highestpriority)
Taxonomic diversity Phylogenetic diversity Functional diversity
Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino
000
025
050
075
100
Charismatic megafauna
Con
serv
atio
n pr
iorit
y (0
to 1
)
F IGURE 5emspRepresentationoftoppriorityareaswithintheextentofsuitablehabitatofcharismaticspeciesAdecreaseinprioritycorrespondswithincreasingsizeofareasthatneedtobeprotectedForexamplethetop25priorityarearefersto25ofthesizeoftheentirelandscapeandthehighest25ofpriorityscoresfromZonationalgorithmThereforelessproportionoftop-priorityareaoverlappedwiththeextentofsuitablehabitatofthefourcharismaticmegafauna
Rep
rese
ntat
ion
()
Taxonomic diversity Phylogenetic diversity Functional diversity
020
4060
8010
0
Top5 10 17 25 5 10 17 25 5 10 17 25
CombinedTigerElephantOrangutanRhinoceros
8emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
having approximately half of tigers suitable habitat represented lessthanhalfoftheamountofpriorityareascoveredbythetigerCombiningallcharismaticspeciesimprovedtherepresentationofpriorityareasbutonlybyasmallamountcomparedtothetiger(Figure5)Wealsoidenti-fiedpriorityareasthatwerenotcoveredbyanyofthefourcharismaticspeciesrsquodistributionsegforthetop5priorityareas28(taxonomy-basedpriority)8(phylogeny-based)and18(trait-based)wereout-sidetheextentofsuitablehabitatofthecharismaticspecies
Evaluationonthepotentialoftheother180mammalspecies inSumatrainrepresentingpriorityareasrevealedthattheextentofsuit-ablehabitatwasagoodpredictorof surrogacypotential (Figure6)However species with similar size of suitable habitat representedvaryingproportionsofpriorityareasThetigerhadahighersurrogacypotentialcomparedtomostotherspecieswithsimilarsizeofsuitablehabitatTheelephantontheoppositehadanunderperformingsur-rogacypotentialthanwaspredictedbyitssizeofsuitablehabitat
4emsp |emspDISCUSSION
41emsp|emspThe role of the charismatic megafauna in Sumatra as biodiversity surrogates
We used recently developed techniques to evaluate the con-servation effectiveness of using charismatic megafauna as sur-rogates for taxonomic phylogenetic and functional diversity of
SumatranmammalsWefoundthatSumatrantigerhadthehigh-estsurrogacypotentialbecausemostof theco-occurringmam-malswerewellrepresentedwithinitsdistributionanditcoveredhigh amounts of priority areas for the three biodiversity facets(taxonomicphylogeneticandfunctionaldiversity)Thisisrelatedto its relatively large distribution compared to the other char-ismatic species in Sumatra However the tiger also had highersurrogacypotentialthanpredictedbasedonitsdistributionsizealoneThissupportsthefindingfromapreviousstudythatlargepredators have important surrogate roles for other mammals(Thorntonetal2016)
The Sumatran elephant had the second highest potential as asurrogatespecies inSumatra intermsoftherepresentationofco-occurringspeciesHoweveritcoveredalowerproportionofpriorityareasthanexpectedbyitsrangesizebecauseitdidnotoccurinmostofwesternmountainrangeswheremostofthepriorityareaswerefoundTheorangutanand rhinoceros represented relatively loweramountsoftotalpriorityareaswhichmatchedwiththeirrestricteddistributionrangeHoweveralmosttheentirerangesofthesetwospeciesencompassedtop-rankedpriorityareasThisimpliesallocat-ingconservationresourcestoprotectareaswithintherangeoftheorangutanandtherhinowouldresult inahighcontributiontotheprotectionofbroaderbiodiversitybutthisstrategyalonewilllikelybeinsufficientforSumatranbiodiversitygiventherestricteddistri-butionofthetwospecies
F IGURE 6emspTherepresentationoftop5priorityareastop10priorityareastop17priorityareasandtop25priorityareaswithinthesuitablehabitatofcharismaticmegafaunarelativetotheirextentofsuitablehabitatLettersintheplotandtheorangepointsindicatethecharismaticmegafaunaspeciesT=tigerE=AsianelephantO=SumatranorangutanR=SumatranrhinocerosGreypointsindicatetheothermammalspeciesinSumatra(180species)Bluelinesrepresentfittedvaluesofpriorityarearepresentationbasedongeneralisedadditivemodels
1 2 3 4 5
020
4060
80
Taxonomic diversity
T
OR
ETop
5
1 2 3 4 5
Phylogenetic diversity
T
OR
E
1 2 3 4 5
Functional diversity
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
10
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
17
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
25
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
Rep
rese
ntat
ion
()
log(suitable area [km sq])
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
R E FE R E N C E S
AndelmanSJampFaganWF(2000)UmbrellasandflagshipsEfficientconservation surrogates or expensivemistakesProceedings of the National Academy of Science of the United States of America97(11)5954ndash5959httpsdoiorg101073pnas100126797
BadanPusatStatistik(2012)Indonesianpopulationbasedonprovinces19711980199019952000and2010Retrievedfromwwwbpsgoid
Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
4emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
In the spatial prioritisation analysis we only used areas of highhabitat suitability to represent theoccurrenceof the species (here-after ldquoextent of suitable habitatrdquo) becausewe intendedwanted theresulting conservation area systems to include areaswhere speciesaremost likelytopersistOfthe193nativeterrestrialmammalspe-cies inSumatra thetworecentlysplitorangutanpopulations (Nateretal2017)wereconsideredasonespeciesandeightspecieswerenotmodelledbyRondininietal(2011)thereforeouranalysisincludedatotalof184species(includingthefourcharismaticspecies)
23emsp|emspAssessing the representation of mammal species by the charismatic megafauna
Weassessedthesurrogacypotentialofcharismaticmegafaunaspe-cies by overlaying their extent of suitable habitatwith that of allothermammals Representationwas calculated as the proportionof a speciesrsquo extent of suitable habitat overlappingwith thehabi-tatofeachcharismaticmegafaunaspeciesWeperformedall spa-tialdataprocessingusing therpackages ldquosprdquo (PebesmaampBivand2005)andldquorasterrdquo(HijmansampvanEtten2012)inrversion341(RDevelopmentCoreTeam2008)
24emsp|emspAssessing the representation of priority areas based on multiple facets of biodiversity
We identified conservation priority areas using the Zonation v4software(Moilanenetal2014)TheinputdataforZonationanaly-sisarerastermapsofbiodiversityfeatures(egspeciesandhabitattypes)whichrepresenttheirspatialdistributionTheZonationalgo-rithmstarts from the full extentof the landscapeof interest andtheniterativelyremovesareaswiththelowestvalueforconserva-tionbasedontheoccurrencelevelofbiodiversityfeatures(Moilanenetal2005)Thisiterativeremovalprocessgeneratesamapshow-ing a hierarchic ranking of conservation priorities throughout thelandscape(MoilanenKujalaampLeathwick2009)Eachrastercelloftheoutputmap contains a rankof conservationpriorities rangingbetween0(lowestpriority)and1(highestpriority)thatcanbevisu-alisedasahierarchicalzonedmapoftoppriorityareasforconserva-tionZonationhasalreadybeenusedforassessingumbrellaeffectsofsurrogatespecies(DiMininampMoilanen2014)andexaminingcon-gruencyofpriority areas formultiple facetsofbiodiversity (Brumetal2017PollockThuillerampJetz2017StreckerOldenWhittierampPaukert2011)
We used Core Area Zonation as the cell removal rules inZonationwhichranksthecellsacrossthe landscapebasedonthemost importantoccurrenceof a feature andhencecould identifycore areas of features in biodiversity-poor areas (Moilanen etal2014)We also incorporated connectivity considerations by usingthe Boundary Length Penalty to produce more compact reservesolutions (MoilanenampWintle2007)We ran three separate anal-yses to identify priorities for threedifferent biodiversity facets aspecies-level analysis (taxonomic prioritisation) an analysis basedonphylogeneticgroups(phylogeneticprioritisation)andananalysis
basedonfunctionalgroups(functionalprioritisation)Furthertech-nicaldetailsareprovidedinAppendixS2
25emsp|emspBiodiversity features for spatial prioritisation
Weusedindividualspeciesasthebiodiversityfeaturesforthespa-tialprioritisationbasedontaxonomicdiversityWeperformedarea-weighted resampling to scaleup thehabitat suitabilitymaps fromtheoriginal300mresolutionto1kmWeusedaresolutionof1kmas a compromise between computational time and relevance forconservationmanagement on the islandWeweighted14 speciesendemictoSumatratwiceasmuchasthenon-endemicspeciestorepresentthehigherglobalvalueoftheirconservationontheislandWealsoperformedasensitivityanalysisonalternativeweightingofendemicspeciesbuttheresultsshowednosubstantialdifferences(seeAppendixS4)
For spatial prioritisation based on phylogenetic diversity wedefined phylogenetic groups following the framework developedbyStreckeretal(2011)andBrumetal(2017)Weusedthemam-malian phylogenetic supertree created by Bininda-Emonds etal(2007)andupdatedbyFritzBininda-EmondsandPurvis(2009)tocreateaphylogeneticdistancematrixamong181mammalspeciesinSumatraafterexcludingthreespecieswhichwerenotavailablein themammaliansupertreeWethenperformedprincipalcoordi-nateanalysisonthephylogeneticdistancematrixandselectedthefirst16eigenvectorswhichexplainedgt1oftotalvariationTheseeigenvectors altogether accounted for 69 of the total variationEacheigenvectorwassplitinto10quantiles(seeAppendixS4forthesensitivitytest)andthenconverted intobinaryvariablesOurquantileswerewiderthanthoseusedinBrumetal(2017)becausewe had fewer number of species in Sumatra To represent phylo-geneticgroups inspatialmapswecreatedabinarymatrixofspe-ciestimesphylogeneticgroupArea-weightedhabitatsuitabilitymapsat1kmresolutionwerereclassifiedintobinarymapswithathresholdof005 (this threshold reduces the riskof introducingcommissionerrorswithoutpenalisingspecieswithnarrowhabitatdistributions)andthenwereconvertedintogridtimesspeciesmatrixFinallywemul-tipliedthetwomatricestoobtaingridtimesphylogeneticgroupsmatrixinwhichagridcellcontainedthenumberofspeciesbelongingtoaparticularphylogenetic groupWe thengenerated spatialmapsofphylogeneticgroupdistributionfromthismatrix
Wemappedmammalianfunctionaltraitswithsimilarprocedurewithphylogeny-basedprioritisationusing life-history traitsasop-posed to phylogenetic eigenvectorsWe selected five life-historyand ecological categories represented by nine traits adult bodymassmaximumlongevityreproductivespeed(weaningagegesta-tionlength)reproductionoutput(neonatebodymasslittersizeandlittersperyear)andresourceuse(trophiclevelandhabitatbreadth)WeusedtheglobaldatasetforterrestrialmammaltraitscompiledbyPacificietal (2013)andDiMarcoandSantini (2015)fromvarioussourcessuchasPanTHERIA(Jonesetal2009)andAnAge(Tacutuetal2013)Weassignedthepresenceabsenceofeachlevelofcate-goricaltraitsinabinarymatrixofspeciestimestraitWesplitcontinuous
emspensp emsp | emsp5Journal of Applied EcologySIBARANI et Al
traitsinto10quantilesandweassignedpresenceabsenceofeachsame-sizetraitleveltospeciesNextwemultipliedthegridtimesspe-ciesmatrixwithspeciestimestraitmatrixWeconvertedtheresultingmatrixofgridtimestraitintospatialmapsoffunctionaltraitlevelsThedetailedprocedureofdatapreparationisprovidedinAppendixS2
Werantheprioritisationanalysisseparatelyusingspeciesrsquohabi-tatsuitabilitymapsasinputsintaxonomy-basedprioritisationphy-logeneticgroupmapsinphylogeny-basedprioritisationandlevelsoffunctionaltraitsintrait-basedprioritisationWethenextractedthe
top51017and25ofpriorityareasforeachprioritisationscenariosandoverlaid themwith theextentof suitablehabitatofthecharismaticmegafaunaspeciesWemeasuredthesurrogacypo-tentialofcharismaticmegafaunaastheproportionofpriorityareasacrossSumatrathatoverlappedwiththeextentofsuitablehabitatofthespeciesunderconsiderationInadditionwealsocalculatedthesurrogacypotentialsofothermammal species inSumatra tocom-pare the performance of the four charismatic megafauna specieswiththatofotherspecies
F IGURE 2emspTherepresentationoftheco-occurringmammalspecieswithinthesuitablehabitatofcharismaticmegafauna(a)overalland(b)categorisedaccordingtotheirIUCNRedListcategoriesDDDataDeficientLCLeastConcernNTNearThreatenedVUVulnerableENEndangeredCRCriticallyEndangeredNotethatthescalesofy-axisof(b)aredifferentacrossthefourcharismaticmegafaunaspecies
TigerE
lephantO
rangutanR
hinoceros
0 25 50 75 100
0
50
100
150
0
50
100
150
0
50
100
150
0
50
100
150
Representation ()
Num
ber o
f spe
cies
Tiger Elephant Orangutan Rhinoceros
0 25 50 75 100 0 25 50 75 0 20 40 60 80 0 3 6 9
DD (N = 13)
LC (N = 110)
NT (N = 20)
VU (N = 26)
EN (N = 12)
CR (N = 3)
Representation ()
IUC
N R
ed L
ist c
ateg
orie
s
(a)
(b)
6emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
3emsp |emspRESULTS
31emsp|emspSurrogacy for terrestrial mammal species
Among the four charismaticmegafauna species the tiger had thehighest spatial overlap with other mammal species represent-ingameanof52 (SD=27)of theextentof suitablehabitatofother Sumatranmammals (Figure2) The representation levels forothercharismatic speciesweremuch lower18 for theelephant(SD=12) 9 for the orangutan (SD=11) and 2 for the rhi-noceros(SD=2)Onlytwospecieshadahighspatialoverlapwiththeelephant(ie93forthelesserlarge-footedmyotisMyotis has-seltii and85 for thebig-earedhorseshoebatRhinolophus macro-tis)Likewiseonly twospecieshadahighspatialoverlapwith theorangutan(ie81forthebig-earedhorseshoebatand71forthepen-tailedtreeshrewPtilocercus lowii)
Mostofthesuitablehabitatfororangutanandrhinocerosover-lappedwiththetigerbutonly41oftheelephantsextentofsuit-ablehabitatoverlappedwiththetigersThesuitablehabitatfortigeroverlappedsubstantially(52)withthecriticallyendangeredSundapangolin Manis javanica Of the 12 endangered species (Figure2)onlyonewasunderrepresentedbythetigeriethehairy-nosedotter
Lutra sumatranawithrepresentationlevelof12Theother11en-dangeredspecieswerewellrepresentedbythetigerwiththeover-laprangingfrom40to89Combiningthefoursurrogatespeciesonlyimprovedtherepresentationlevelsbyameanof5(SD=6range=0ndash12)comparedtotheperformanceofthetigeralone
32emsp|emspSurrogacy for priority areas based on multiple facets of biodiversity
Wediscoveredsubstantialspatialmismatchesamongtheareasiden-tifiedundertaxonomicphylogeneticandfunctionaldiversityprior-itisation scenarios (Figure3)When looking at the top5priorityareasforeachbiodiversityfacetswhichaltogetherencompassedanareaof21595km2we foundanoverlapofonly3227km2 (15)acrossthethreefacetsPriorityareassharedamongthethreeprior-itisationscenariosmostlyoccurredinhighlandsofnorthernSumatraandwesternmountainrangesIntaxonomy-basedprioritisationthepriorityareasweremorespreadoutacrosstheislandincludingcen-tral lowlandandeasterncoastsThespatial solution forprioritisa-tionbasedonphylogeneticgroupswasmoreclumpedinthewesternhalfoftheislandPriorityareasforconservingfunctionaltraitswere
F IGURE 3emspPriorityconservationareasinSumatrabasedonmultiplefacetsofbiodiversityThetopmapsreportthespatialprioritisationresultsreportingtherankingofconservationprioritythroughoutthelandscape(with0meaninglowestimportanceand1meaninghighestimportance)WecategorisedhighpriorityareasintofourgroupsofnestedpriorityrankingsTop5(valuesofgt095)top10(gt090)top17(gt083)andtop25(gt075)Theinsetmapsreportthespatialdistributionofcharismaticmegafaunaspecies
Priority rankingTop 5Top 10Top 17Top 25
Taxonomic diversity Phylogenetic diversity Functional diversity
Maps of charismaticmegafauna species
Tiger Elephant Orangutan Rhinoceros
0 400200 km
Extent of suitable habitat
emspensp emsp | emsp7Journal of Applied EcologySIBARANI et Al
morecongruenttophylogeny-based(20overlap)thantaxonomy-basedprioritisation(17overlap)
Ingeneralmostoftheextentofsuitablehabitatofthecharis-maticspecieswasofhighconservationpriority(Figure4)Theorang-utanandrhinoceroscoveredareasinSumatrawithrelativelyhigherconservationpriorityranksthanthetigerandelephantAmongthefour elephant had the most variability in representing conserva-tionprioritiesegfortaxonomicprioritisationIQRelephant=044
IQRtiger=023 IQRorangutan=010 IQRrhinoceros=005 (com-pletesummarystatisticsinAppendixS4)
Whilemostofthesuitablehabitatsfortheorangutanandrhinoc-erosoverlappedwithareasofhighconservationprioritytheseonlyac-countedforsmallproportionoftoppriorityareasgiventherestricteddistributionofthesespecies(Figure5)Thetigerssuitablehabitathadthehighestarealcoverageofpriorityareasforthethreebiodiversityfac-etsanditrepresentedphylogeneticprioritiesparticularlywellElephant
F IGURE 4emspBoxplotsshowingthevariationofconservationpriorityrankswithintheextentofsuitablehabitatofcharismaticmegafaunaspecies The y-axisrepresentstheconservationpriorityranksthatwerecomputedbasedoniterativecellremovalprocessofZonationrangingfrom0(lowestpriority)to1(highestpriority)
Taxonomic diversity Phylogenetic diversity Functional diversity
Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino
000
025
050
075
100
Charismatic megafauna
Con
serv
atio
n pr
iorit
y (0
to 1
)
F IGURE 5emspRepresentationoftoppriorityareaswithintheextentofsuitablehabitatofcharismaticspeciesAdecreaseinprioritycorrespondswithincreasingsizeofareasthatneedtobeprotectedForexamplethetop25priorityarearefersto25ofthesizeoftheentirelandscapeandthehighest25ofpriorityscoresfromZonationalgorithmThereforelessproportionoftop-priorityareaoverlappedwiththeextentofsuitablehabitatofthefourcharismaticmegafauna
Rep
rese
ntat
ion
()
Taxonomic diversity Phylogenetic diversity Functional diversity
020
4060
8010
0
Top5 10 17 25 5 10 17 25 5 10 17 25
CombinedTigerElephantOrangutanRhinoceros
8emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
having approximately half of tigers suitable habitat represented lessthanhalfoftheamountofpriorityareascoveredbythetigerCombiningallcharismaticspeciesimprovedtherepresentationofpriorityareasbutonlybyasmallamountcomparedtothetiger(Figure5)Wealsoidenti-fiedpriorityareasthatwerenotcoveredbyanyofthefourcharismaticspeciesrsquodistributionsegforthetop5priorityareas28(taxonomy-basedpriority)8(phylogeny-based)and18(trait-based)wereout-sidetheextentofsuitablehabitatofthecharismaticspecies
Evaluationonthepotentialoftheother180mammalspecies inSumatrainrepresentingpriorityareasrevealedthattheextentofsuit-ablehabitatwasagoodpredictorof surrogacypotential (Figure6)However species with similar size of suitable habitat representedvaryingproportionsofpriorityareasThetigerhadahighersurrogacypotentialcomparedtomostotherspecieswithsimilarsizeofsuitablehabitatTheelephantontheoppositehadanunderperformingsur-rogacypotentialthanwaspredictedbyitssizeofsuitablehabitat
4emsp |emspDISCUSSION
41emsp|emspThe role of the charismatic megafauna in Sumatra as biodiversity surrogates
We used recently developed techniques to evaluate the con-servation effectiveness of using charismatic megafauna as sur-rogates for taxonomic phylogenetic and functional diversity of
SumatranmammalsWefoundthatSumatrantigerhadthehigh-estsurrogacypotentialbecausemostof theco-occurringmam-malswerewellrepresentedwithinitsdistributionanditcoveredhigh amounts of priority areas for the three biodiversity facets(taxonomicphylogeneticandfunctionaldiversity)Thisisrelatedto its relatively large distribution compared to the other char-ismatic species in Sumatra However the tiger also had highersurrogacypotentialthanpredictedbasedonitsdistributionsizealoneThissupportsthefindingfromapreviousstudythatlargepredators have important surrogate roles for other mammals(Thorntonetal2016)
The Sumatran elephant had the second highest potential as asurrogatespecies inSumatra intermsoftherepresentationofco-occurringspeciesHoweveritcoveredalowerproportionofpriorityareasthanexpectedbyitsrangesizebecauseitdidnotoccurinmostofwesternmountainrangeswheremostofthepriorityareaswerefoundTheorangutanand rhinoceros represented relatively loweramountsoftotalpriorityareaswhichmatchedwiththeirrestricteddistributionrangeHoweveralmosttheentirerangesofthesetwospeciesencompassedtop-rankedpriorityareasThisimpliesallocat-ingconservationresourcestoprotectareaswithintherangeoftheorangutanandtherhinowouldresult inahighcontributiontotheprotectionofbroaderbiodiversitybutthisstrategyalonewilllikelybeinsufficientforSumatranbiodiversitygiventherestricteddistri-butionofthetwospecies
F IGURE 6emspTherepresentationoftop5priorityareastop10priorityareastop17priorityareasandtop25priorityareaswithinthesuitablehabitatofcharismaticmegafaunarelativetotheirextentofsuitablehabitatLettersintheplotandtheorangepointsindicatethecharismaticmegafaunaspeciesT=tigerE=AsianelephantO=SumatranorangutanR=SumatranrhinocerosGreypointsindicatetheothermammalspeciesinSumatra(180species)Bluelinesrepresentfittedvaluesofpriorityarearepresentationbasedongeneralisedadditivemodels
1 2 3 4 5
020
4060
80
Taxonomic diversity
T
OR
ETop
5
1 2 3 4 5
Phylogenetic diversity
T
OR
E
1 2 3 4 5
Functional diversity
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
10
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
17
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
25
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
Rep
rese
ntat
ion
()
log(suitable area [km sq])
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
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BadanPusatStatistik(2012)Indonesianpopulationbasedonprovinces19711980199019952000and2010Retrievedfromwwwbpsgoid
Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
emspensp emsp | emsp5Journal of Applied EcologySIBARANI et Al
traitsinto10quantilesandweassignedpresenceabsenceofeachsame-sizetraitleveltospeciesNextwemultipliedthegridtimesspe-ciesmatrixwithspeciestimestraitmatrixWeconvertedtheresultingmatrixofgridtimestraitintospatialmapsoffunctionaltraitlevelsThedetailedprocedureofdatapreparationisprovidedinAppendixS2
Werantheprioritisationanalysisseparatelyusingspeciesrsquohabi-tatsuitabilitymapsasinputsintaxonomy-basedprioritisationphy-logeneticgroupmapsinphylogeny-basedprioritisationandlevelsoffunctionaltraitsintrait-basedprioritisationWethenextractedthe
top51017and25ofpriorityareasforeachprioritisationscenariosandoverlaid themwith theextentof suitablehabitatofthecharismaticmegafaunaspeciesWemeasuredthesurrogacypo-tentialofcharismaticmegafaunaastheproportionofpriorityareasacrossSumatrathatoverlappedwiththeextentofsuitablehabitatofthespeciesunderconsiderationInadditionwealsocalculatedthesurrogacypotentialsofothermammal species inSumatra tocom-pare the performance of the four charismatic megafauna specieswiththatofotherspecies
F IGURE 2emspTherepresentationoftheco-occurringmammalspecieswithinthesuitablehabitatofcharismaticmegafauna(a)overalland(b)categorisedaccordingtotheirIUCNRedListcategoriesDDDataDeficientLCLeastConcernNTNearThreatenedVUVulnerableENEndangeredCRCriticallyEndangeredNotethatthescalesofy-axisof(b)aredifferentacrossthefourcharismaticmegafaunaspecies
TigerE
lephantO
rangutanR
hinoceros
0 25 50 75 100
0
50
100
150
0
50
100
150
0
50
100
150
0
50
100
150
Representation ()
Num
ber o
f spe
cies
Tiger Elephant Orangutan Rhinoceros
0 25 50 75 100 0 25 50 75 0 20 40 60 80 0 3 6 9
DD (N = 13)
LC (N = 110)
NT (N = 20)
VU (N = 26)
EN (N = 12)
CR (N = 3)
Representation ()
IUC
N R
ed L
ist c
ateg
orie
s
(a)
(b)
6emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
3emsp |emspRESULTS
31emsp|emspSurrogacy for terrestrial mammal species
Among the four charismaticmegafauna species the tiger had thehighest spatial overlap with other mammal species represent-ingameanof52 (SD=27)of theextentof suitablehabitatofother Sumatranmammals (Figure2) The representation levels forothercharismatic speciesweremuch lower18 for theelephant(SD=12) 9 for the orangutan (SD=11) and 2 for the rhi-noceros(SD=2)Onlytwospecieshadahighspatialoverlapwiththeelephant(ie93forthelesserlarge-footedmyotisMyotis has-seltii and85 for thebig-earedhorseshoebatRhinolophus macro-tis)Likewiseonly twospecieshadahighspatialoverlapwith theorangutan(ie81forthebig-earedhorseshoebatand71forthepen-tailedtreeshrewPtilocercus lowii)
Mostofthesuitablehabitatfororangutanandrhinocerosover-lappedwiththetigerbutonly41oftheelephantsextentofsuit-ablehabitatoverlappedwiththetigersThesuitablehabitatfortigeroverlappedsubstantially(52)withthecriticallyendangeredSundapangolin Manis javanica Of the 12 endangered species (Figure2)onlyonewasunderrepresentedbythetigeriethehairy-nosedotter
Lutra sumatranawithrepresentationlevelof12Theother11en-dangeredspecieswerewellrepresentedbythetigerwiththeover-laprangingfrom40to89Combiningthefoursurrogatespeciesonlyimprovedtherepresentationlevelsbyameanof5(SD=6range=0ndash12)comparedtotheperformanceofthetigeralone
32emsp|emspSurrogacy for priority areas based on multiple facets of biodiversity
Wediscoveredsubstantialspatialmismatchesamongtheareasiden-tifiedundertaxonomicphylogeneticandfunctionaldiversityprior-itisation scenarios (Figure3)When looking at the top5priorityareasforeachbiodiversityfacetswhichaltogetherencompassedanareaof21595km2we foundanoverlapofonly3227km2 (15)acrossthethreefacetsPriorityareassharedamongthethreeprior-itisationscenariosmostlyoccurredinhighlandsofnorthernSumatraandwesternmountainrangesIntaxonomy-basedprioritisationthepriorityareasweremorespreadoutacrosstheislandincludingcen-tral lowlandandeasterncoastsThespatial solution forprioritisa-tionbasedonphylogeneticgroupswasmoreclumpedinthewesternhalfoftheislandPriorityareasforconservingfunctionaltraitswere
F IGURE 3emspPriorityconservationareasinSumatrabasedonmultiplefacetsofbiodiversityThetopmapsreportthespatialprioritisationresultsreportingtherankingofconservationprioritythroughoutthelandscape(with0meaninglowestimportanceand1meaninghighestimportance)WecategorisedhighpriorityareasintofourgroupsofnestedpriorityrankingsTop5(valuesofgt095)top10(gt090)top17(gt083)andtop25(gt075)Theinsetmapsreportthespatialdistributionofcharismaticmegafaunaspecies
Priority rankingTop 5Top 10Top 17Top 25
Taxonomic diversity Phylogenetic diversity Functional diversity
Maps of charismaticmegafauna species
Tiger Elephant Orangutan Rhinoceros
0 400200 km
Extent of suitable habitat
emspensp emsp | emsp7Journal of Applied EcologySIBARANI et Al
morecongruenttophylogeny-based(20overlap)thantaxonomy-basedprioritisation(17overlap)
Ingeneralmostoftheextentofsuitablehabitatofthecharis-maticspecieswasofhighconservationpriority(Figure4)Theorang-utanandrhinoceroscoveredareasinSumatrawithrelativelyhigherconservationpriorityranksthanthetigerandelephantAmongthefour elephant had the most variability in representing conserva-tionprioritiesegfortaxonomicprioritisationIQRelephant=044
IQRtiger=023 IQRorangutan=010 IQRrhinoceros=005 (com-pletesummarystatisticsinAppendixS4)
Whilemostofthesuitablehabitatsfortheorangutanandrhinoc-erosoverlappedwithareasofhighconservationprioritytheseonlyac-countedforsmallproportionoftoppriorityareasgiventherestricteddistributionofthesespecies(Figure5)Thetigerssuitablehabitathadthehighestarealcoverageofpriorityareasforthethreebiodiversityfac-etsanditrepresentedphylogeneticprioritiesparticularlywellElephant
F IGURE 4emspBoxplotsshowingthevariationofconservationpriorityrankswithintheextentofsuitablehabitatofcharismaticmegafaunaspecies The y-axisrepresentstheconservationpriorityranksthatwerecomputedbasedoniterativecellremovalprocessofZonationrangingfrom0(lowestpriority)to1(highestpriority)
Taxonomic diversity Phylogenetic diversity Functional diversity
Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino
000
025
050
075
100
Charismatic megafauna
Con
serv
atio
n pr
iorit
y (0
to 1
)
F IGURE 5emspRepresentationoftoppriorityareaswithintheextentofsuitablehabitatofcharismaticspeciesAdecreaseinprioritycorrespondswithincreasingsizeofareasthatneedtobeprotectedForexamplethetop25priorityarearefersto25ofthesizeoftheentirelandscapeandthehighest25ofpriorityscoresfromZonationalgorithmThereforelessproportionoftop-priorityareaoverlappedwiththeextentofsuitablehabitatofthefourcharismaticmegafauna
Rep
rese
ntat
ion
()
Taxonomic diversity Phylogenetic diversity Functional diversity
020
4060
8010
0
Top5 10 17 25 5 10 17 25 5 10 17 25
CombinedTigerElephantOrangutanRhinoceros
8emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
having approximately half of tigers suitable habitat represented lessthanhalfoftheamountofpriorityareascoveredbythetigerCombiningallcharismaticspeciesimprovedtherepresentationofpriorityareasbutonlybyasmallamountcomparedtothetiger(Figure5)Wealsoidenti-fiedpriorityareasthatwerenotcoveredbyanyofthefourcharismaticspeciesrsquodistributionsegforthetop5priorityareas28(taxonomy-basedpriority)8(phylogeny-based)and18(trait-based)wereout-sidetheextentofsuitablehabitatofthecharismaticspecies
Evaluationonthepotentialoftheother180mammalspecies inSumatrainrepresentingpriorityareasrevealedthattheextentofsuit-ablehabitatwasagoodpredictorof surrogacypotential (Figure6)However species with similar size of suitable habitat representedvaryingproportionsofpriorityareasThetigerhadahighersurrogacypotentialcomparedtomostotherspecieswithsimilarsizeofsuitablehabitatTheelephantontheoppositehadanunderperformingsur-rogacypotentialthanwaspredictedbyitssizeofsuitablehabitat
4emsp |emspDISCUSSION
41emsp|emspThe role of the charismatic megafauna in Sumatra as biodiversity surrogates
We used recently developed techniques to evaluate the con-servation effectiveness of using charismatic megafauna as sur-rogates for taxonomic phylogenetic and functional diversity of
SumatranmammalsWefoundthatSumatrantigerhadthehigh-estsurrogacypotentialbecausemostof theco-occurringmam-malswerewellrepresentedwithinitsdistributionanditcoveredhigh amounts of priority areas for the three biodiversity facets(taxonomicphylogeneticandfunctionaldiversity)Thisisrelatedto its relatively large distribution compared to the other char-ismatic species in Sumatra However the tiger also had highersurrogacypotentialthanpredictedbasedonitsdistributionsizealoneThissupportsthefindingfromapreviousstudythatlargepredators have important surrogate roles for other mammals(Thorntonetal2016)
The Sumatran elephant had the second highest potential as asurrogatespecies inSumatra intermsoftherepresentationofco-occurringspeciesHoweveritcoveredalowerproportionofpriorityareasthanexpectedbyitsrangesizebecauseitdidnotoccurinmostofwesternmountainrangeswheremostofthepriorityareaswerefoundTheorangutanand rhinoceros represented relatively loweramountsoftotalpriorityareaswhichmatchedwiththeirrestricteddistributionrangeHoweveralmosttheentirerangesofthesetwospeciesencompassedtop-rankedpriorityareasThisimpliesallocat-ingconservationresourcestoprotectareaswithintherangeoftheorangutanandtherhinowouldresult inahighcontributiontotheprotectionofbroaderbiodiversitybutthisstrategyalonewilllikelybeinsufficientforSumatranbiodiversitygiventherestricteddistri-butionofthetwospecies
F IGURE 6emspTherepresentationoftop5priorityareastop10priorityareastop17priorityareasandtop25priorityareaswithinthesuitablehabitatofcharismaticmegafaunarelativetotheirextentofsuitablehabitatLettersintheplotandtheorangepointsindicatethecharismaticmegafaunaspeciesT=tigerE=AsianelephantO=SumatranorangutanR=SumatranrhinocerosGreypointsindicatetheothermammalspeciesinSumatra(180species)Bluelinesrepresentfittedvaluesofpriorityarearepresentationbasedongeneralisedadditivemodels
1 2 3 4 5
020
4060
80
Taxonomic diversity
T
OR
ETop
5
1 2 3 4 5
Phylogenetic diversity
T
OR
E
1 2 3 4 5
Functional diversity
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
10
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
17
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
25
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
Rep
rese
ntat
ion
()
log(suitable area [km sq])
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
R E FE R E N C E S
AndelmanSJampFaganWF(2000)UmbrellasandflagshipsEfficientconservation surrogates or expensivemistakesProceedings of the National Academy of Science of the United States of America97(11)5954ndash5959httpsdoiorg101073pnas100126797
BadanPusatStatistik(2012)Indonesianpopulationbasedonprovinces19711980199019952000and2010Retrievedfromwwwbpsgoid
Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
6emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
3emsp |emspRESULTS
31emsp|emspSurrogacy for terrestrial mammal species
Among the four charismaticmegafauna species the tiger had thehighest spatial overlap with other mammal species represent-ingameanof52 (SD=27)of theextentof suitablehabitatofother Sumatranmammals (Figure2) The representation levels forothercharismatic speciesweremuch lower18 for theelephant(SD=12) 9 for the orangutan (SD=11) and 2 for the rhi-noceros(SD=2)Onlytwospecieshadahighspatialoverlapwiththeelephant(ie93forthelesserlarge-footedmyotisMyotis has-seltii and85 for thebig-earedhorseshoebatRhinolophus macro-tis)Likewiseonly twospecieshadahighspatialoverlapwith theorangutan(ie81forthebig-earedhorseshoebatand71forthepen-tailedtreeshrewPtilocercus lowii)
Mostofthesuitablehabitatfororangutanandrhinocerosover-lappedwiththetigerbutonly41oftheelephantsextentofsuit-ablehabitatoverlappedwiththetigersThesuitablehabitatfortigeroverlappedsubstantially(52)withthecriticallyendangeredSundapangolin Manis javanica Of the 12 endangered species (Figure2)onlyonewasunderrepresentedbythetigeriethehairy-nosedotter
Lutra sumatranawithrepresentationlevelof12Theother11en-dangeredspecieswerewellrepresentedbythetigerwiththeover-laprangingfrom40to89Combiningthefoursurrogatespeciesonlyimprovedtherepresentationlevelsbyameanof5(SD=6range=0ndash12)comparedtotheperformanceofthetigeralone
32emsp|emspSurrogacy for priority areas based on multiple facets of biodiversity
Wediscoveredsubstantialspatialmismatchesamongtheareasiden-tifiedundertaxonomicphylogeneticandfunctionaldiversityprior-itisation scenarios (Figure3)When looking at the top5priorityareasforeachbiodiversityfacetswhichaltogetherencompassedanareaof21595km2we foundanoverlapofonly3227km2 (15)acrossthethreefacetsPriorityareassharedamongthethreeprior-itisationscenariosmostlyoccurredinhighlandsofnorthernSumatraandwesternmountainrangesIntaxonomy-basedprioritisationthepriorityareasweremorespreadoutacrosstheislandincludingcen-tral lowlandandeasterncoastsThespatial solution forprioritisa-tionbasedonphylogeneticgroupswasmoreclumpedinthewesternhalfoftheislandPriorityareasforconservingfunctionaltraitswere
F IGURE 3emspPriorityconservationareasinSumatrabasedonmultiplefacetsofbiodiversityThetopmapsreportthespatialprioritisationresultsreportingtherankingofconservationprioritythroughoutthelandscape(with0meaninglowestimportanceand1meaninghighestimportance)WecategorisedhighpriorityareasintofourgroupsofnestedpriorityrankingsTop5(valuesofgt095)top10(gt090)top17(gt083)andtop25(gt075)Theinsetmapsreportthespatialdistributionofcharismaticmegafaunaspecies
Priority rankingTop 5Top 10Top 17Top 25
Taxonomic diversity Phylogenetic diversity Functional diversity
Maps of charismaticmegafauna species
Tiger Elephant Orangutan Rhinoceros
0 400200 km
Extent of suitable habitat
emspensp emsp | emsp7Journal of Applied EcologySIBARANI et Al
morecongruenttophylogeny-based(20overlap)thantaxonomy-basedprioritisation(17overlap)
Ingeneralmostoftheextentofsuitablehabitatofthecharis-maticspecieswasofhighconservationpriority(Figure4)Theorang-utanandrhinoceroscoveredareasinSumatrawithrelativelyhigherconservationpriorityranksthanthetigerandelephantAmongthefour elephant had the most variability in representing conserva-tionprioritiesegfortaxonomicprioritisationIQRelephant=044
IQRtiger=023 IQRorangutan=010 IQRrhinoceros=005 (com-pletesummarystatisticsinAppendixS4)
Whilemostofthesuitablehabitatsfortheorangutanandrhinoc-erosoverlappedwithareasofhighconservationprioritytheseonlyac-countedforsmallproportionoftoppriorityareasgiventherestricteddistributionofthesespecies(Figure5)Thetigerssuitablehabitathadthehighestarealcoverageofpriorityareasforthethreebiodiversityfac-etsanditrepresentedphylogeneticprioritiesparticularlywellElephant
F IGURE 4emspBoxplotsshowingthevariationofconservationpriorityrankswithintheextentofsuitablehabitatofcharismaticmegafaunaspecies The y-axisrepresentstheconservationpriorityranksthatwerecomputedbasedoniterativecellremovalprocessofZonationrangingfrom0(lowestpriority)to1(highestpriority)
Taxonomic diversity Phylogenetic diversity Functional diversity
Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino
000
025
050
075
100
Charismatic megafauna
Con
serv
atio
n pr
iorit
y (0
to 1
)
F IGURE 5emspRepresentationoftoppriorityareaswithintheextentofsuitablehabitatofcharismaticspeciesAdecreaseinprioritycorrespondswithincreasingsizeofareasthatneedtobeprotectedForexamplethetop25priorityarearefersto25ofthesizeoftheentirelandscapeandthehighest25ofpriorityscoresfromZonationalgorithmThereforelessproportionoftop-priorityareaoverlappedwiththeextentofsuitablehabitatofthefourcharismaticmegafauna
Rep
rese
ntat
ion
()
Taxonomic diversity Phylogenetic diversity Functional diversity
020
4060
8010
0
Top5 10 17 25 5 10 17 25 5 10 17 25
CombinedTigerElephantOrangutanRhinoceros
8emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
having approximately half of tigers suitable habitat represented lessthanhalfoftheamountofpriorityareascoveredbythetigerCombiningallcharismaticspeciesimprovedtherepresentationofpriorityareasbutonlybyasmallamountcomparedtothetiger(Figure5)Wealsoidenti-fiedpriorityareasthatwerenotcoveredbyanyofthefourcharismaticspeciesrsquodistributionsegforthetop5priorityareas28(taxonomy-basedpriority)8(phylogeny-based)and18(trait-based)wereout-sidetheextentofsuitablehabitatofthecharismaticspecies
Evaluationonthepotentialoftheother180mammalspecies inSumatrainrepresentingpriorityareasrevealedthattheextentofsuit-ablehabitatwasagoodpredictorof surrogacypotential (Figure6)However species with similar size of suitable habitat representedvaryingproportionsofpriorityareasThetigerhadahighersurrogacypotentialcomparedtomostotherspecieswithsimilarsizeofsuitablehabitatTheelephantontheoppositehadanunderperformingsur-rogacypotentialthanwaspredictedbyitssizeofsuitablehabitat
4emsp |emspDISCUSSION
41emsp|emspThe role of the charismatic megafauna in Sumatra as biodiversity surrogates
We used recently developed techniques to evaluate the con-servation effectiveness of using charismatic megafauna as sur-rogates for taxonomic phylogenetic and functional diversity of
SumatranmammalsWefoundthatSumatrantigerhadthehigh-estsurrogacypotentialbecausemostof theco-occurringmam-malswerewellrepresentedwithinitsdistributionanditcoveredhigh amounts of priority areas for the three biodiversity facets(taxonomicphylogeneticandfunctionaldiversity)Thisisrelatedto its relatively large distribution compared to the other char-ismatic species in Sumatra However the tiger also had highersurrogacypotentialthanpredictedbasedonitsdistributionsizealoneThissupportsthefindingfromapreviousstudythatlargepredators have important surrogate roles for other mammals(Thorntonetal2016)
The Sumatran elephant had the second highest potential as asurrogatespecies inSumatra intermsoftherepresentationofco-occurringspeciesHoweveritcoveredalowerproportionofpriorityareasthanexpectedbyitsrangesizebecauseitdidnotoccurinmostofwesternmountainrangeswheremostofthepriorityareaswerefoundTheorangutanand rhinoceros represented relatively loweramountsoftotalpriorityareaswhichmatchedwiththeirrestricteddistributionrangeHoweveralmosttheentirerangesofthesetwospeciesencompassedtop-rankedpriorityareasThisimpliesallocat-ingconservationresourcestoprotectareaswithintherangeoftheorangutanandtherhinowouldresult inahighcontributiontotheprotectionofbroaderbiodiversitybutthisstrategyalonewilllikelybeinsufficientforSumatranbiodiversitygiventherestricteddistri-butionofthetwospecies
F IGURE 6emspTherepresentationoftop5priorityareastop10priorityareastop17priorityareasandtop25priorityareaswithinthesuitablehabitatofcharismaticmegafaunarelativetotheirextentofsuitablehabitatLettersintheplotandtheorangepointsindicatethecharismaticmegafaunaspeciesT=tigerE=AsianelephantO=SumatranorangutanR=SumatranrhinocerosGreypointsindicatetheothermammalspeciesinSumatra(180species)Bluelinesrepresentfittedvaluesofpriorityarearepresentationbasedongeneralisedadditivemodels
1 2 3 4 5
020
4060
80
Taxonomic diversity
T
OR
ETop
5
1 2 3 4 5
Phylogenetic diversity
T
OR
E
1 2 3 4 5
Functional diversity
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
10
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
17
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
25
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
Rep
rese
ntat
ion
()
log(suitable area [km sq])
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
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Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
emspensp emsp | emsp7Journal of Applied EcologySIBARANI et Al
morecongruenttophylogeny-based(20overlap)thantaxonomy-basedprioritisation(17overlap)
Ingeneralmostoftheextentofsuitablehabitatofthecharis-maticspecieswasofhighconservationpriority(Figure4)Theorang-utanandrhinoceroscoveredareasinSumatrawithrelativelyhigherconservationpriorityranksthanthetigerandelephantAmongthefour elephant had the most variability in representing conserva-tionprioritiesegfortaxonomicprioritisationIQRelephant=044
IQRtiger=023 IQRorangutan=010 IQRrhinoceros=005 (com-pletesummarystatisticsinAppendixS4)
Whilemostofthesuitablehabitatsfortheorangutanandrhinoc-erosoverlappedwithareasofhighconservationprioritytheseonlyac-countedforsmallproportionoftoppriorityareasgiventherestricteddistributionofthesespecies(Figure5)Thetigerssuitablehabitathadthehighestarealcoverageofpriorityareasforthethreebiodiversityfac-etsanditrepresentedphylogeneticprioritiesparticularlywellElephant
F IGURE 4emspBoxplotsshowingthevariationofconservationpriorityrankswithintheextentofsuitablehabitatofcharismaticmegafaunaspecies The y-axisrepresentstheconservationpriorityranksthatwerecomputedbasedoniterativecellremovalprocessofZonationrangingfrom0(lowestpriority)to1(highestpriority)
Taxonomic diversity Phylogenetic diversity Functional diversity
Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino Tiger Elephant Orangutan Rhino
000
025
050
075
100
Charismatic megafauna
Con
serv
atio
n pr
iorit
y (0
to 1
)
F IGURE 5emspRepresentationoftoppriorityareaswithintheextentofsuitablehabitatofcharismaticspeciesAdecreaseinprioritycorrespondswithincreasingsizeofareasthatneedtobeprotectedForexamplethetop25priorityarearefersto25ofthesizeoftheentirelandscapeandthehighest25ofpriorityscoresfromZonationalgorithmThereforelessproportionoftop-priorityareaoverlappedwiththeextentofsuitablehabitatofthefourcharismaticmegafauna
Rep
rese
ntat
ion
()
Taxonomic diversity Phylogenetic diversity Functional diversity
020
4060
8010
0
Top5 10 17 25 5 10 17 25 5 10 17 25
CombinedTigerElephantOrangutanRhinoceros
8emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
having approximately half of tigers suitable habitat represented lessthanhalfoftheamountofpriorityareascoveredbythetigerCombiningallcharismaticspeciesimprovedtherepresentationofpriorityareasbutonlybyasmallamountcomparedtothetiger(Figure5)Wealsoidenti-fiedpriorityareasthatwerenotcoveredbyanyofthefourcharismaticspeciesrsquodistributionsegforthetop5priorityareas28(taxonomy-basedpriority)8(phylogeny-based)and18(trait-based)wereout-sidetheextentofsuitablehabitatofthecharismaticspecies
Evaluationonthepotentialoftheother180mammalspecies inSumatrainrepresentingpriorityareasrevealedthattheextentofsuit-ablehabitatwasagoodpredictorof surrogacypotential (Figure6)However species with similar size of suitable habitat representedvaryingproportionsofpriorityareasThetigerhadahighersurrogacypotentialcomparedtomostotherspecieswithsimilarsizeofsuitablehabitatTheelephantontheoppositehadanunderperformingsur-rogacypotentialthanwaspredictedbyitssizeofsuitablehabitat
4emsp |emspDISCUSSION
41emsp|emspThe role of the charismatic megafauna in Sumatra as biodiversity surrogates
We used recently developed techniques to evaluate the con-servation effectiveness of using charismatic megafauna as sur-rogates for taxonomic phylogenetic and functional diversity of
SumatranmammalsWefoundthatSumatrantigerhadthehigh-estsurrogacypotentialbecausemostof theco-occurringmam-malswerewellrepresentedwithinitsdistributionanditcoveredhigh amounts of priority areas for the three biodiversity facets(taxonomicphylogeneticandfunctionaldiversity)Thisisrelatedto its relatively large distribution compared to the other char-ismatic species in Sumatra However the tiger also had highersurrogacypotentialthanpredictedbasedonitsdistributionsizealoneThissupportsthefindingfromapreviousstudythatlargepredators have important surrogate roles for other mammals(Thorntonetal2016)
The Sumatran elephant had the second highest potential as asurrogatespecies inSumatra intermsoftherepresentationofco-occurringspeciesHoweveritcoveredalowerproportionofpriorityareasthanexpectedbyitsrangesizebecauseitdidnotoccurinmostofwesternmountainrangeswheremostofthepriorityareaswerefoundTheorangutanand rhinoceros represented relatively loweramountsoftotalpriorityareaswhichmatchedwiththeirrestricteddistributionrangeHoweveralmosttheentirerangesofthesetwospeciesencompassedtop-rankedpriorityareasThisimpliesallocat-ingconservationresourcestoprotectareaswithintherangeoftheorangutanandtherhinowouldresult inahighcontributiontotheprotectionofbroaderbiodiversitybutthisstrategyalonewilllikelybeinsufficientforSumatranbiodiversitygiventherestricteddistri-butionofthetwospecies
F IGURE 6emspTherepresentationoftop5priorityareastop10priorityareastop17priorityareasandtop25priorityareaswithinthesuitablehabitatofcharismaticmegafaunarelativetotheirextentofsuitablehabitatLettersintheplotandtheorangepointsindicatethecharismaticmegafaunaspeciesT=tigerE=AsianelephantO=SumatranorangutanR=SumatranrhinocerosGreypointsindicatetheothermammalspeciesinSumatra(180species)Bluelinesrepresentfittedvaluesofpriorityarearepresentationbasedongeneralisedadditivemodels
1 2 3 4 5
020
4060
80
Taxonomic diversity
T
OR
ETop
5
1 2 3 4 5
Phylogenetic diversity
T
OR
E
1 2 3 4 5
Functional diversity
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
10
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
17
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
25
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
Rep
rese
ntat
ion
()
log(suitable area [km sq])
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
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Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
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DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
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HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
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IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
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MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
8emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
having approximately half of tigers suitable habitat represented lessthanhalfoftheamountofpriorityareascoveredbythetigerCombiningallcharismaticspeciesimprovedtherepresentationofpriorityareasbutonlybyasmallamountcomparedtothetiger(Figure5)Wealsoidenti-fiedpriorityareasthatwerenotcoveredbyanyofthefourcharismaticspeciesrsquodistributionsegforthetop5priorityareas28(taxonomy-basedpriority)8(phylogeny-based)and18(trait-based)wereout-sidetheextentofsuitablehabitatofthecharismaticspecies
Evaluationonthepotentialoftheother180mammalspecies inSumatrainrepresentingpriorityareasrevealedthattheextentofsuit-ablehabitatwasagoodpredictorof surrogacypotential (Figure6)However species with similar size of suitable habitat representedvaryingproportionsofpriorityareasThetigerhadahighersurrogacypotentialcomparedtomostotherspecieswithsimilarsizeofsuitablehabitatTheelephantontheoppositehadanunderperformingsur-rogacypotentialthanwaspredictedbyitssizeofsuitablehabitat
4emsp |emspDISCUSSION
41emsp|emspThe role of the charismatic megafauna in Sumatra as biodiversity surrogates
We used recently developed techniques to evaluate the con-servation effectiveness of using charismatic megafauna as sur-rogates for taxonomic phylogenetic and functional diversity of
SumatranmammalsWefoundthatSumatrantigerhadthehigh-estsurrogacypotentialbecausemostof theco-occurringmam-malswerewellrepresentedwithinitsdistributionanditcoveredhigh amounts of priority areas for the three biodiversity facets(taxonomicphylogeneticandfunctionaldiversity)Thisisrelatedto its relatively large distribution compared to the other char-ismatic species in Sumatra However the tiger also had highersurrogacypotentialthanpredictedbasedonitsdistributionsizealoneThissupportsthefindingfromapreviousstudythatlargepredators have important surrogate roles for other mammals(Thorntonetal2016)
The Sumatran elephant had the second highest potential as asurrogatespecies inSumatra intermsoftherepresentationofco-occurringspeciesHoweveritcoveredalowerproportionofpriorityareasthanexpectedbyitsrangesizebecauseitdidnotoccurinmostofwesternmountainrangeswheremostofthepriorityareaswerefoundTheorangutanand rhinoceros represented relatively loweramountsoftotalpriorityareaswhichmatchedwiththeirrestricteddistributionrangeHoweveralmosttheentirerangesofthesetwospeciesencompassedtop-rankedpriorityareasThisimpliesallocat-ingconservationresourcestoprotectareaswithintherangeoftheorangutanandtherhinowouldresult inahighcontributiontotheprotectionofbroaderbiodiversitybutthisstrategyalonewilllikelybeinsufficientforSumatranbiodiversitygiventherestricteddistri-butionofthetwospecies
F IGURE 6emspTherepresentationoftop5priorityareastop10priorityareastop17priorityareasandtop25priorityareaswithinthesuitablehabitatofcharismaticmegafaunarelativetotheirextentofsuitablehabitatLettersintheplotandtheorangepointsindicatethecharismaticmegafaunaspeciesT=tigerE=AsianelephantO=SumatranorangutanR=SumatranrhinocerosGreypointsindicatetheothermammalspeciesinSumatra(180species)Bluelinesrepresentfittedvaluesofpriorityarearepresentationbasedongeneralisedadditivemodels
1 2 3 4 5
020
4060
80
Taxonomic diversity
T
OR
ETop
5
1 2 3 4 5
Phylogenetic diversity
T
OR
E
1 2 3 4 5
Functional diversity
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
10
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
17
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
1 2 3 4 5
020
4060
80
T
OR
ETop
25
1 2 3 4 5
T
OR
E
1 2 3 4 5
T
OR
E
Rep
rese
ntat
ion
()
log(suitable area [km sq])
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
R E FE R E N C E S
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BadanPusatStatistik(2012)Indonesianpopulationbasedonprovinces19711980199019952000and2010Retrievedfromwwwbpsgoid
Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
emspensp emsp | emsp9Journal of Applied EcologySIBARANI et Al
The combination of spatial prioritisation and surrogacy anal-ysis allowed us to identify areas within the charismatic speciesrsquohabitatswithhighand lowconservationprioritiesThechoiceofflagship speciesdependson thebroad conservation goals of thepeopledevelopingthemarketingcampaignandthepreferencesoftheirtargetaudiencessoouranalysisshouldnotbeusedtoprior-itise conservation effort between flagships Insteadwe proposethe use of spatial conservation prioritisation techniques to iden-tifyareaswithintherangesofcharismaticmegafaunaspeciesthatalsoprovidebenefitstothebroaderbiodiversityConsideringthatcharismaticmegafaunadidnotrepresentthewholeextentofiden-tified priority areas even with all species combined our resultssuggestthatconservationmanagersandpolicymakersinSumatrashouldprotectimportantareasforbiodiversitythatoccuroutsidetherangeofcharismaticspeciesOurfindingsagreewithpreviouswork suggesting that targeting charismaticmegafauna in conser-vationisnotenoughtoachievebroaderbiodiversityconservationtargets yet the benefit of their protection can be improved byusingwell-surveyedtaxonomicgroupsandhabitattypes(DiMininampMoilanen2014)
Habitatsuitabilitymodelsusedinthisstudyareamoreaccuratedepiction of species distributions compared to geographic ranges(IUCN range maps) because unsuitable habitats have been ex-cludedfromthedistribution(RondininiWilsonBoitaniGranthamampPossingham2006)However suitablehabitat is notnecessarilytranslatedintospeciespresenceasspeciesmaybeextirpatedfromitssuitablehabitatduetohuman-causeddisturbancesThisissuecanbeaddressedbyperforminghabitatsuitabilitymodelvalidationforallspeciesconsideredinthestudyordevelopinginductivespeciesdistributionmodelsasinputfeaturesforfuturestudyThishoweverrequirescollectingoccurrencedataforallconsideredspecieswhicharenotcurrentlyavailableInthisstudyweonlyconsideredmam-maliandiversityduetodataavailabilityalongallbiodiversityfacetsFuturework is still necessary to incorporate other vertebrate in-vertebrateandplanttaxainspatialconservationplanning(DiMarcoetal2017)Moreoverwhileourstudywasonlyaimedatidentify-ingimportantareasforbiodiversity(andhowtheserelatetocharis-maticspecies)thereareotherfactorsthatneedtobeconsideredtomaximisetheconservationeffectivenessofselectedpriorityareassuchasthepresenceofthreateningprocessesandthecostofunder-takingconservationactions
42emsp|emspWhat should we conserve Integrating the conservation of charismatic species and the multiple facets of biodiversity
Charismaticspecieshavebeenthefocusofmanyconservationor-ganisations both to allocate funding and define priorities for ac-tionsWhile it is importanttoreduceextinctionrisksfacedbytheendangered charismatic species there are also many threatenednon-charismatic species that play vital ecosystem functions orareevolutionarydistinctbutoften receive littleprotection (IsaacTurvey CollenWaterman amp Baillie 2007) Simply assuming that
protecting thehabitatsof charismaticmegafauna specieswill alsoprovideco-benefitstotherestofbiodiversitycanleadtotheextinc-tionofunderstudiedspecies
The use of taxonomic diversity alone for identifying conser-vationpriorities has beenquestioned and regarded as inadequatebecause it fails to representdistinctivenessamongspecies (Vane-WrightHumphriesampWilliams1991)Ofthetop5priorityareasinSumatrawefoundthatonly15(3227km2)wasspatiallycon-gruentamongthetaxonomicphylogeneticandfunctionaldiversitywhileatotalofnearly13000km2wouldberequiredtorepresenttoppriorityareasunderallbiodiversityfacetsThisimpliesthattheuseofonlyonebiodiversityfacetinconservationplanningcouldresultinthefailuretomaintaintheotheraspectsSpeciesaretheproductsofevolutionaryandecologicalprocesses(BoslashhnampAmundsen2004)andspecies-focusedconservationstrategiesmaybeinsufficienttoguarantee the protection of evolutionary history and themainte-nanceofecosystemfunctioning
Selectingawide-rangingcharismaticspecies todelineatepro-tectedareasofhighbiodiversityimportancecouldbeaneffectivestrategy for protecting broader biodiversityHowever protectingtheentiredistributionofathreatenedcharismaticspeciesischal-lenging and cost-inefficient Therefore we suggest prioritisingthe protection of wide-ranging charismatic speciesrsquo habitats thatalsogive thehighest contribution tootherbiodiversityelementsAlthoughourresultssuggestedthatcombiningthefourcharismaticspeciesonlyslightlyincreasethespatialrepresentationofpriorityareasbasedonamarketingperspectivecampaigns thatcreatealdquoflagship fleetrdquo byusing all four speciesmay appeal to a broadertarget audience and so increase potential funding and support(Veriacutessimoetal2014)
Wealsosuggest it is importanttofollowacomplementaryap-proach integrating as a goal both the protection of charismaticspeciesandtheprotectionofareasofhighbiodiversityimportanceoutside thedistributionof thesespeciesOur results showedthateven protecting an area as small as 1734ndash5949km2 outside thedistributionofthefourcharismaticspecieswouldresult inamuchmorecompletecoverageoftoppriorityareasfortheconservationofthetaxonomicphylogeneticandfunctionaldiversityofSumatranmammalsChoosingnewflagshipspeciesorflagshipfleetfromover-lookedspecieslisttopromotethenewprotectedareasystemsandraise funds (Smith etal 2012) can be awinning strategy for thispurpose This needs amore thorough assessmentwhich includesdecidingthetargetaudienceandformulatingthemarketingstrategy(Verissimoetal2011)
We chose Sumatra as our case study area because it hostssome of the highest global concentrations of terrestrial andthreatenedmammalsandthedistributionofcharismaticspeciesisakeydriverofconservationactionthereThisisespeciallyrel-evantwithinaregion (ieSoutheastAsia) that istodayreceivingproportionally less attention from international conservationjournals than it used to in past decades (DiMarco etal 2017)Biodiversity co-occurring with charismatic species may benefitfromprotectedareaestablishmentand lawenforcementefforts
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
R E FE R E N C E S
AndelmanSJampFaganWF(2000)UmbrellasandflagshipsEfficientconservation surrogates or expensivemistakesProceedings of the National Academy of Science of the United States of America97(11)5954ndash5959httpsdoiorg101073pnas100126797
BadanPusatStatistik(2012)Indonesianpopulationbasedonprovinces19711980199019952000and2010Retrievedfromwwwbpsgoid
Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
10emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
suchaspatrollingtosafeguardtheprotectedareasfromillegalac-tivities(Linkieetal2015)Thereforeourrecommendationisalsorelevant in regions beyond Sumatra where (a) the conservationof charismatic megafauna is prominent and (b) protected areasareenforcedbymeansthatexcludeanyharmfulillegalactivitiesWhilecharismaticmegafaunaareprimarilyprotectedforthesakeof these species conservationdecision-makers should also con-siderbroaderbenefitsforotheraspectsofbiodiversityinconser-vation planning aswe face increasing rate of species extinctionworld-wideOurstudyrevealedaframeworktoplanconservationstrategiesinwhichtheprotectionofcharismaticmegafaunaben-efits broader aspects of biodiversitywe showed the ldquoumbrellardquoeffectivenessofdifferentcharismaticspeciesand identified im-portantbiodiversityareasoutsidethedistributionofcharismaticspeciesusingspatialprioritisationtechniques
Whileitisidealtoprotectallaspectsofbiodiversityimplement-ing systematic conservation planning is challenging especially indevelopingcountrieswherethegrowthrateofhumanpopulationis high land tenure conflicts are prominent and wildlife habitatsarefragmentedBasedonourfindingsweprovideseveralrecom-mendations for conservationmanagers in Sumatra thatmay helpadvancingmoreefficientconservationofmammalsontheisland
1 Enforcementofprotectedareamanagementinplaceswherethereis high overlap between taxonomic phylogenetic and functionaldiversity such as Leuser Landscape and Bukit BarisanMountainRanges especially where the three facets of biodiversity alsooverlap with the habitat of charismatic megafauna species
2 Expansionofcurrentprotectedareasorestablishmentofnewpro-tectedareastocoverunprotectedtoppriorityareasidentifiedinthisstudybyusingtheSumatranldquobigfourrdquotoraisefundsandgainpoliti-calandpublicsupportIfthepriorityareasareoutsidethehabitatoftheldquobigfourrdquonewflagshipspeciesfleetshouldbeidentified
3 Collationanddigitisationofspeciesoccurrencerecordsofalltaxatoenablemorerobustspeciesdistributionmodellingandspatialconservationplanning
ACKNOWLEDG EMENTS
We thank A Reside for the advice in using Zonation Bob SmithananonymousreviewerandtheEditorforconstructivecommentsonthemanuscriptWethanktheIndonesianEndowmentFundforEducation (LPDP)of theMinistryofFinancefor fundingtoMCSSKwassupportedbytheAustralianResearchCouncil
AUTHORSrsquo CONTRIBUTIONS
MCSconceivedtheideasandMCSMDMandSKdesignedthestudyMDMandCRdevelopedandprovidedtheglobalhabi-tat suitabilitymodels for terrestrialmammalsMCS andMDManalysedthedataMCSledthewritingandallauthorscontributedinthewritingofthemanuscriptAllauthorscontributedcriticallytothedraftsandgavefinalapprovalforpublication
DATA ACCE SSIBILIT Y
Data available via the Dryad Digital Repository httpsdoiorg105061dryad6n0b28n(SibaraniDiMarcoRondininiampKark2019)
ORCID
Marsya C Sibarani httporcidorg0000-0003-0942-139X
Moreno Di Marco httpsorcidorg0000-0002-8902-4193
Carlo Rondinini httpsorcidorg0000-0002-6617-018X
Salit Kark httpsorcidorg0000-0002-7183-3988
R E FE R E N C E S
AndelmanSJampFaganWF(2000)UmbrellasandflagshipsEfficientconservation surrogates or expensivemistakesProceedings of the National Academy of Science of the United States of America97(11)5954ndash5959httpsdoiorg101073pnas100126797
BadanPusatStatistik(2012)Indonesianpopulationbasedonprovinces19711980199019952000and2010Retrievedfromwwwbpsgoid
Bininda-EmondsORPCardilloM JonesKEMacpheeRDEBeck RMD Grenyer R hellip Purvis A (2007) The delayed riseof present-daymammalsNature446(7135) 507ndash512 httpsdoiorg101038nature05634
BoslashhnTampAmundsenP-A(2004)EcologicalinteractionsandevolutionForgottenpartsofbiodiversityBioScience54(9)804ndash805httpsdoiorg1016410006-3568(2004)054[0804eiaefp]20co2
BottrillMCJosephLNCarwardineJBodeMCookCGameEThellipPossinghamHP (2008) Isconservation triage just smartdecisionmakingTrends in Ecology and Evolution23(12) 649ndash654httpsdoiorg101016jtree200807007
BrumFTGrahamCHCostaGCHedgesSBPenoneCRadeloffV C hellipDavidson AD (2017) Global priorities for conservationacross multiple dimensions of mammalian diversity Proceedings of the National Academy of Science of the United States of Americas114(29)7641ndash7646httpsdoiorg101073pnas1706461114
Caro TM (2010)Conservation by proxy Indicator umbrella keystone flagship and other surrogate speciesWashingtonDCIslandPress
DevictorVMouillotDMeynardCJiguetFThuillerWampMouquetN (2010) Spatial mismatch and congruence between taxonomicphylogeneticandfunctionaldiversityTheneedforintegrativecon-servationstrategiesinachangingworldEcology Letters13(8)1030ndash1040httpsdoiorg101111j1461-0248201001493x
DiMarcoMChapmanSAlthorGKearneySBesanconCButtNhellipWatsonJEM(2017)ChangingtrendsandpersistingbiasesinthreedecadesofconservationscienceGlobal Ecology and Conservation1032ndash42httpsdoiorg101016jgecco201701008
DiMarcoMampSantiniL(2015)Humanpressurespredictspeciesrsquogeo-graphicrangesizebetterthanbiologicaltraitsGlobal Change Biology21(6)2169ndash2178httpsdoiorg101111gcb12834
DiMininEampMoilanenA(2014)Improvingthesurrogacyeffective-nessofcharismaticmegafaunawithwell-surveyedtaxonomicgroupsandhabitattypesJournal of Applied Ecology51(2)281ndash288httpsdoiorg1011111365-266412203
Faith D P (1992) Conservation evaluation and phylogenetic diver-sity Biological Conservation 61(1) 1ndash10 httpsdoiorg1010160006-3207(92)91201-3
FritzSABininda-EmondsORPampPurvisA(2009)Geographicalvariation in predictors of mammalian extinction risk Big is bad
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
emspensp emsp | emsp11Journal of Applied EcologySIBARANI et Al
butonly in thetropicsEcology Letters12(6)538ndash549httpsdoiorg101111j1461-0248200901307x
GADM(2009)Globaladministrativeareasversion10Retrievedfromwwwgadmorg
HijmansR Jamp van Etten J (2012) rasterGeographic analysis andmodelingwithrasterdataRpackageversion20-12
IsaacNJBTurveySTCollenBWatermanCampBaillieJEM(2007) Mammals on the EDGE Conservation priorities based onthreatandphylogenyPLoS ONE2(3)e296httpsdoiorg101371journalpone0000296
IUCN(2016)TheIUCNredlistofthreatenedspeciesVersion2016-1Retrievedfromhttpwwwiucnredlistorg
Jones K E Bielby J Cardillo M Fritz S A ODell J OrmeC D L hellip Purvis A (2009) PanTHERIA A species-level da-tabase of life history ecology and geography of extant andrecently extinct mammals Ecology 90(9) 2648 httpsdoiorg10189008-14941
Joseph LNMaloney R F amp PossinghamH P (2009)Optimal al-locationofresourcesamongthreatenedspeciesAprojectprioriti-zation protocol Conservation Biology 23(2) 328ndash338 httpsdoiorg101111j1523-1739200801124x
Li B V amp Pimm S L (2016) Chinas endemic vertebrates shelteringunder the protective umbrella of the giant panda Conservation Biology30(2)329ndash339httpsdoiorg101111cobi12618
LinkieMMartyrDJHariharARisdiantoDNugrahaRTMaryatihellip Wong W-M (2015) Safeguarding Sumatran tigers Evaluatingeffectiveness of law enforcement patrols and local informant net-works Journal of Applied Ecology 52(4) 851ndash860 httpsdoiorg1011111365-266412461
MargonoBATurubanovaSZhuravlevaIPotapovPampTyukavinaA (2012) Mapping and monitoring deforestation and forest deg-radationinSumatra(Indonesia)usingLandsattimeseriesdatasetsfrom 1990 to 2010 Environmental Research Letters 7(3) 034010httpsdoiorg1010881748-932673034010
MazelFGuilhaumonFMouquetNDevictorVGravelDRenaudJ hellip Thuiller W (2014) Multifaceted diversity-area relationshipsreveal global hotspots ofmammalian species trait and lineage di-versityGlobal Ecology and Biogeography23(8)836ndash847httpsdoiorg101111geb12158
MinistryofForestryoftheRepublicofIndonesia(2007)Strategyandac-tionplanfortheconservationofrhinosinIndonesiaRetrievedfromhttpwwwrhinoresourcecentercompdf_files1341347679274pdf
MoilanenAFrancoAMAEarlyRIFoxRWintleBampThomasCD (2005)Prioritisingmultipleuse landscapes for conservationMethods for largemulti species planning problemsProceedings of the Royal Society of London Series B Biological Sciences272(1575)1885ndash1891httpsdoiorg101098rspb20053164
MoilanenAKujalaHampLeathwickJR(2009)TheZonationframe-work and software for conservationprioritization InAMoilanenKAWilsonampHPPossingham (Eds)Spatial conservation priori-tization Quantitative methods amp computational tools (pp 196ndash210)OxfordOxfordUniversityPress
MoilanenAPouzolsFMMellerLVeachVArponenALeppaumlnenJampKujalaH(2014)Spatial conservation planning methods and soft-ware ZONATION User manualHelsinkiC-BIGConservationBiologyInformaticsGroupUniversityofHelsinki
MoilanenAampWintleBA (2007)Theboundary-qualitypenaltyAquantitativemethod for approximating species responses to frag-mentationinreserveselectionConservation Biology21(2)355ndash364httpsdoiorg101111j1523-1739200600625x
Nater A Mattle-Greminger M P Nurcahyo A Nowak M G deManuel M Desai T hellip Kruumltzen M (2017) Morphometric be-havioral and genomic evidence for a new orangutan species
Current Biology 27(22) 3487ndash3498e10 httpsdoiorg101016jcub201709047
PacificiMSantiniLDiMarcoMBaiseroDFrancucciLGrottoloMarasini G hellip Rondinini C (2013) Generation length for mam-mals Nature Conservation 5 89ndash94 httpsdoiorg103897natureconservation55734
PebesmaEJampBivandRS (2005)ClassesandmethodsforspatialdatainRThesppackageR News5(2)9ndash13
PetcheyOLampGastonKJ(2006)FunctionaldiversityBacktoba-sicsandlookingforwardEcology Letters9(6)741ndash758httpsdoiorg101111j1461-0248200600924x
PHKA (2015) Pembangunan area perlindungan intensif (IntensiveProtection Zone) di TamanNasional Bukit Barisan Selatan sebagaiupayapeningkatanpopulasibadakSumateraRepublicofIndonesiaDirjenPHKAMinistryofForestry
Pollock L J ThuillerWamp JetzW (2017) Large conservationgainspossibleforglobalbiodiversity facetsNature546(7656)141ndash144httpsdoiorg101038nature22368
RDevelopmentCoreTeam(2008)RAlanguageandenvironmentforstatisticalcomputingRetrievedfromhttpwwwr-projectorg
RobergeJ-MampAngelstamP(2004)Usefulnessoftheumbrellaspe-ciesconceptasaconservationtoolConservation Biology18(1)76ndash85httpsdoiorg101111j1523-1739200400450x
Rondinini C Di Marco M Chiozza F Santulli G Baisero DViscontiPhellipBoitaniL(2011)GlobalhabitatsuitabilitymodelsofterrestrialmammalsPhilosophical Transactions of the Royal Society B Biological Sciences 366 2633ndash2641 httpsdoiorg101098rstb20110113
RondininiCWilsonKABoitaniLGranthamHampPossinghamHP(2006)TradeoffsofdifferenttypesofspeciesoccurrencedataforuseinsystematicconservationplanningEcology Letters9(10)1136ndash1145httpsdoiorg101111j1461-0248200600970x
SibaraniMCDiMarcoMRondininiCampKarkS(2019)DatafromMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamega-diverse island Dryad Digital Repository httpsdoiorg105061dryad6n0b28n
SmithRJVeriacutessimoDIsaacNJBampJonesKE(2012)IdentifyingCinderella species Uncovering mammals with conservation flag-ship appeal Conservation Letters 5(3) 205ndash212 httpsdoiorg101111j1755-263X201200229x
SoehartonoTSusiloHDAndayaniNUtamiAtmokoSSSihiteJSalehCampSutrisnoA (2007)Strategi dan rencana aksi konservasi orangutan Indonesia 2007ndash2017Republicof IndonesiaDepartmentofForestry
SoehartonoTSusiloHDSitompulAFGunaryadiDPurastutiEMAzmiWhellipStremmeC (2007)Strategi dan rencana aksi kon-servasi gajah sumatera dan gajah kalimantan 2007ndash2017 Republic of IndonesiaDepartmentofForestry
Soehartono T Wibisono H T Sunarto Martyr D Susilo H DMaddoxTampPriatnaD(2007)Strategi dan rencana aksi konservasi harimau sumatera (2007ndash2017)DepartmentofForestryRepublicofIndonesia
StreckerALOldenJDWhittierJBampPaukertCP(2011)DefiningconservationprioritiesforfreshwaterfishesaccordingtotaxonomicfunctionalandphylogeneticdiversityEcological Applications21(8)3002ndash3013httpsdoiorg10189011-05991
TacutuRCraigTBudovskyAWuttkeDLehmannGTaranukhaDhellipDeMagalhatildeesJP(2013)HumanAgeingGenomicResourcesIntegrateddatabasesandtoolsforthebiologyandgeneticsofageingNucleic Acids Research41(D1)1027ndash1033httpsdoiorg101093nargks1155
Thornton D Zeller K Rondinini C Boitani L Kevin C BurdetteC hellip Quigley H (2016) Assessing the umbrella value of a
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
12emsp |emsp emspenspJournal of Applied Ecology SIBARANI et Al
range-wideconservationnetworkforjaguars(Panthera onca)Ecological Applications26(4)1112ndash1124httpsdoiorg10189015-0602
Vane-WrightR IHumphriesC JampWilliamsPH (1991)What toprotectSystematicsandtheagonyofchoiceBiological Conservation55(3)235ndash254httpsdoiorg1010160006-3207(91)90030-D
VeriacutessimoDFraserIGiratildeoWCamposAASmithRJampMacmillanD C (2014) Evaluating conservation flagships and flagship fleetsConservation Letters7(3)263ndash270httpsdoiorg101111conl12070
VerissimoDMacMillanDCampSmithRJ(2011)TowardasystematicapproachforidentifyingconservationflagshipsConservation Letters4(1)1ndash8httpsdoiorg101111j1755-263X201000151x
Williams PH BurgessNDampRahbekC (2000) Flagship speciesecological complementarity and conserving the diversity of mam-mals and birds in sub- Saharan Africa Animal Conservation3(3)249ndash260httpsdoiorg101017S1367943000000974
SUPPORTING INFORMATION
Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle
How to cite this articleSibaraniMCDiMarcoMRondininiCKarkSMeasuringthesurrogacypotentialofcharismaticmegafaunaspeciesacrosstaxonomicphylogeneticandfunctionaldiversityonamegadiverseislandJ Appl Ecol 2019001ndash12 httpsdoiorg1011111365-266413360
![Rethinking megafauna - CentAURcentaur.reading.ac.uk/89222/1/Moleon_et_al_2020_ProcB.pdf · 2021. 7. 9. · 86 megafauna [6-7], the ubiquity of the megafauna concept in addressing](https://img.pdfslide.net/doc/110x75/613e8c8669193359046d3023/rethinking-megafauna-2021-7-9-86-megafauna-6-7-the-ubiquity-of-the-megafauna.jpg)
