decreasing brown bear (ursus arctos) habitat due to climate...

Ecology and Evolution 2018811887ndash11899 emsp|emsp11887wwwecolevolorg

Received24March2018emsp |emsp Revised29August2018emsp |emsp Accepted25September2018DOI101002ece34645

O R I G I N A L R E S E A R C H

Decreasing brown bear (Ursus arctos) habitat due to climate change in Central Asia and the Asian Highlands

Junhu Su12 emsp|emspAchyut Aryal23 emsp|emspIbrahim M Hegab124emsp|emsp Uttam Babu Shrestha5emsp|emspSean C P Coogan67emsp|emspSambandam Sathyakumar8emsp|emsp Munkhnast Dalannast9emsp|emspZhigang Dou10emsp|emspYila Suo10emsp|emspXilite Dabu10emsp|emsp Hongyan Fu10emsp|emspLiji Wu10emsp|emspWeihong Ji123

1CollegeofGrasslandScienceKeyLaboratoryofGrasslandEcosystem(MinistryofEducation)GansuAgriculturalUniversityLanzhouChina2GansuAgriculturalUniversityndashMasseyUniversityResearchCentreforGrasslandBiodiversityGansuAgriculturalUniversityLanzhouChina3InstituteofNaturalandMathematicalSciencesMasseyUniversityAucklandNewZealand4DepartmentofHygieneZoonosesandAnimalBehaviourampManagementFacultyofVeterinaryMedicineSuezCanalUniversityIsmailiaEgypt5InstituteforAgricultureandtheEnvironmentUniversityofSouthernQueenslandToowoombaQLDAustralia6TheCharlesPerkinsCentreSchoolofBiologicalSciencesTheUniversityofSydneySydneyAustralia7TheDepartmentofRenewableResourcesUniversityofAlbertaEdmontonABCanada8WildlifeInstituteofIndiaChandrabaniIndia9BatsResearchCenterofMongoliaUlaanbaatarMongolia10GansuYanchiwanNationalNatureReserveBureauSubeiChina

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsEcology and EvolutionpublishedbyJohnWileyampSonsLtd

CorrespondenceWeihongJiInstituteofNaturalandMathematicalSciencesMasseyUniversityAlbanyPrivateBag102904NorthShoreMailCentreAucklandNewZealandGansuAgriculturalUniversityndashMasseyUniversityResearchCentreforGrasslandBiodiversityGansuAgriculturalUniversityLanzhouChinaEmailjjweihongmasseyacnz

Funding informationInternationalCooperationResearchProgrammeofMasseyUniversityResearchFundGrantAwardNumberGAMU-RCGB-1401ldquoFuxiTalentrdquoPlanofGansuAgriculturalUniversityunderGrantGrantAwardNumberGaufx-02J03GansuProvincialNaturalScienceFoundationforDistinguishedYoungScholarsofChinaGrantAwardNumber1606RJDA314AlertisFundforNatureConservationNetherlandsandTalentedYoungScientistsfellowship(TYSP)oftheMinistryofScienceandTechnologyofChinaSpecialfundsfordisciplineconstructionofGansuAgriculturalUniversityGrantAwardNumberGSAU-XKJS-2018-003NationalNaturalScience

AbstractAroundtheworldclimatechangehasimpactedmanyspeciesInthisstudyweusedbioclimaticvariablesandbiophysicallayersofCentralAsiaandtheAsianHighlandscombinedwithpresencedataofbrownbear(Ursus arctos)tounderstandtheircurrentdistribution andpredict their future distribution under the current rate of climatechangeOurbioclimaticmodelshowedthatthecurrentsuitablehabitatofbrownbearencompasses3430493km2inthestudyareathemajorityofwhich(gt65)locatedinChinaOuranalysesdemonstrated that suitablehabitatwillbe reducedby11(37886130km2)acrossCentralAsiaandtheAsianHighlandsby2050duetocli-matechangepredominantly(gt90)duetothechangesintemperatureandprecipita-tion The spatially averaged mean annual temperature of brown bear habitat iscurrentlyminus12degCandpredictedtoincreaseto16degCby2050Meanannualprecipita-tioninbrownbearhabitatsispredictedtoincreaseby13(from406to459mm)by2050 Such changes in two critical climatic variables may significantly affect thebrownbeardistributionethologicalrepertoiresandphysiologicalprocesseswhichmayincreasetheirriskofextirpationinsomeareasApproximately32(1124330km2)ofthetotalsuitablehabitatfallswithinprotectedareaswhichwaspredictedtore-duceto1103912km2(18loss)by2050Futurelossofsuitablehabitatsinsidethe

11888emsp |emsp emspensp SU et al

1emsp |emspINTRODUC TION

Around the world climate change has had significant direct andindirect impacts on terrestrial species by being amajor cause ofspeciationandspeciesextirpation(PoundampSalzmann2017)Manystudieshaverecentlyfocusedontheecological(EttersonampMazer2016WikelskiampTertitski2016)ethological (MunozMarquezampReal2015)andbiologicalchanges(Torres-Diazetal2016Hulme2016) in relation to climatic change For example various ecosys-tems are vulnerable to climate changewhichmay induce a broadarrayofadverseeffectssuchasdisturbancesofphenologicaleventsfoodwebdisruptionspathogensanddiseasespreadandultimatelyinworstcasescenariosmayincludeextinctionrisks(WuLuZhouChenampXu2016)Furthermoreclimatechangehasimpactedspe-cies distributions by reducing and fragmenting of the area of ani-malhabitats(ChenHillOhlemullerRoyampThomas2011Loarieetal2008LordampWhitlatch2015Lundhedeetal2014SuAryalNanampJi2015Wu2016)Howevertotacklethechallengeofthechangingclimaticconditionsspecieshaveadopteddifferentmech-anisms to counteract themagnitude and speed of climate changeeitherindividuallyorwithinapopulation(HillGriffithsampThomas2011)Forexamplenaturalpopulationsmayreacttoclimatechangeeithercollectivelybyshiftingtheirgeographicalhabitats(Hoffmannamp Sgro 2011) or individually by adjusting their behavioral activi-tiesthroughmodificationsoftheirdietactivityandenergybudgetandreproductivetactics(BellardBertelsmeierLeadleyThuillerampCourchamp2012)Althoughthesetacticalresponseshaveprovento have a short-term efficiency (Crane Roncoli amp Hoogenboom2011)towithstandclimaticchangessomestudiesshowedthatupto42ofspeciesincertaingeographicalareasareatriskofextinc-tioninthelongtermduetodeforestationandhabitatfragmentationsolely(SodhiKohBrookampNg2004)

TheAsianhighlandsthehighmountainousareasofAfghanistanBhutanChinaIndiaMongoliaNepalPakistanandRussiacontainrichbiological diversity andprovide important ecosystem servicesfordownstreamhumancommunitiesThe regionhasalso someofthegreatestspeciesendemismontheplanetandthegreatvariationinclimatetopographyandelevationunderpinsrichculturaldiversity(Xuetal2009)Howeverclimatechangehasgreatlyimpactedbothbiological diversity and ecosystems services in these areas (Aryal

BruntonampRaubenheimer2014KujalaMoilanenAraujoampCabeza2013 Xu et al 2009) The variation of climate effects that havebeendetectedintheAsianHighlandsshowsprogressivesubstantialchangesatseverallevelsfromspeciestoecosystems(YuLuedelingampXu2010)Impactsofclimatechangeonthehydrologybiodiversityandecosystemsinthisareahavebeenreportedwhichincludegla-cialmeltingchangesinstreamflowgroundwaterscarcityaltitudinalshiftsreductioninplantandanimalhabitatsbiodiversitylossandgrasslanddesiccation (PresseyCabezaWattsCowlingampWilson2007ShresthaampBawa2014Waltheretal2002)Furthermoremany studies foresee that future climate changewouldhaveevengreaterimpactsonbiodiversityinCentralAsia(ChenLiDengFangampLi2016GarciaCabezaRahbekampAraujo2014ZhangZhangampSanderson2013)ItisimportanttounderstandtheresultsofthesechangesintermsofhabitatcompositionstructureandfunctionandtheresponsesofanimalgeographicaldistributionwhichcanguideconservationactionsandgovernmenteffortsintheAsianHighlandsinresponsetothesechanges(XuampGrumbine2014)

Brown bear (Ursus arctos) is a solitary non-territorial specieswithapromiscuousorpolygamousmatingsystem(JerinaJonozovicKrofelampSkrbinsek2013Figure1)Ithasacircumglobaldistribu-tion in thenorthernhemisphereoccurring inNorthAmerica (TheUnitedStatesandCanada)EuropeandnorthernandCentralAsia(McLellanetal2008)Manyoftheseregionsareexperiencingrapidclimatechange (ShresthaGautamampBawa2012) InCentralAsiaandtheAsianHighlandsbrownbeardistribution ismostly limitedtohigherelevationareaswheremorepronouncedeffectsofclimatechangehavebeenreported(Aryal2012Aryaletal2014)Intheseregionsbrownbeardistributionandpresencemaybeimpactedbychanging thermal regimes vegetation and prey abundance Suchchangesmaypotentiallyincreasehumanndashbearconflictsduetoshift-ing indistributionof resources andpossibly increasing scarcityofkeyresourcessuchaswaterandfoodInthesamewaydecreaseinspeciesdiversityintheregionduetoclimatechange(BertelsmeierLuqueampCourchamp2013Seimetal2016)mightdirectlyaffectthedistributionandabundanceofthebrownbearbyreducingfoodresources Reduced food abundancemay result in increased inci-dencesofbrownbearsmovingtoanthropogenicareasinsearchoffoodwhichcouldleadtoincreasedlevelsoflivestockdepredationand humanndashbear conflictHowever little is known regarding how

FoundationofChinaGrantAwardNumber31460566and31760706 protectedareasmayforcebrownbearstomoveoutsidetheprotectedareasthereby

increasingtheirriskofmortalityThereforemoreprotectedareasshouldbeestab-lishedinthesuitablebrownbearhabitatsinfuturetosustainpopulationsinthisre-gionFurthermoredevelopmentofcorridorsisneededtoconnecthabitatsbetweenprotectedareasofdifferentcountries inCentralAsiaSuchpracticeswill facilitateclimatemigrationandconnectivityamongpopulationsandmovementbetweenandwithincountries

K E Y W O R D S

AsianhighlandsbrownbearCentralAsiaclimatechangehabitatshiftspeciesdistributionmodel

emspensp emsp | emsp11889SU et al

brownbearshabitatswill be affectedby future climate change inthis regionTodate there are fewpublished studieswhich assessthepotential impactsof climatechangeonbrownbears and theirhabitats(Roberts Nielsen amp Stenhouse 2014) and none in AsiaHowever in recentyears agrowing interest in theecological andevolutionarymechanismsofhabitatchangeduetoclimatechangehaspromoteddevelopmentofnewmodelsforpredictingbiodiver-sityfutures(Anderson2013)Herewemodelthecurrentsuitablehabitats for brown bears and predict the change in their futuredistribution due to climate change in Central Asia and the AsianHighlandsWeusedbioclimaticvariablesandbiophysical layersofCentralAsiacombinedwithpresencedataofbrownbeartounder-standtheircurrentandfuturedistributionSuchinformationwillbehelpful inmanaging brown bear populations and designing futureconservationpoliciesinAsia

2emsp |emspMATERIAL AND METHODS

21emsp|emspStudy area and presence data

Weselected11 countriesofCentralAsia and theAsianHighlandswherebrownbearsarereportedtooccur(McLellanetal2008)ThecountriesincludedareAfghanistanBhutanChinaIndiaKazakhstanKyrgyzstan Mongolia Nepal Pakistan Tajikistan and UzbekistanWe obtained brown bear presence data by field surveys informa-tion frompublishedandunpublishedsourcesandoccurrencedatafrom Global Biodiversity Information Facility (GBIF httpswwwgbiforg)PresencedatawerecollectedthroughfieldsurveysinNepal(2007ndash2011) India (200120062012)Mongolia (2010ndash2014)andChina (2014) In these studies brownbear presencewas recordedbysignsurveyincludingcameratrapsscatsandtracksBrownbearpresenceinformationfrompublishedandunpublishedliteratureswasobtained for India (Sathyakumar 2001 2006 Sathyakumar KaulAshrafMookherjeeampMenon2012)Pakistan(Nawaz2007NawazSwensonampZakaria2008)Mongolia(MccarthyWaitsampMijiddorj

2014) China (Gong amp Harris 2006 Xu 2010) Nepal (Aryal IiiRaubenheimerJiampBrunton2012AryalSathyakumarampSchwartz2010)Kazakhstan(Loginov2012)andAfghanistan(MohebLawsonampMostafawi2012)Additionally informationonbrownbearpres-encerecentkillingpoachingsitesandlocationsofhumanndashbearen-countersandconflictswasobtainedfromlocalauthorities

We used a species distribution map from the InternationalUnion for Conservation of Nature (IUCN McLellan et al 2008IUCNampWildlife Conservation Society 2008) to extract brownbeardistributionareas(resident)forAsiawiththehelpofArcGISWeplottedGPSpointsofcurrentpresencedataweobtainedandcompared with the current IUCN distribution map for groundtruthingforvalidationandcorrectionWedownloadedprotectedareasofAsia(IUCNampUNEP-WCMC2014)andbasedonthelit-erature survey of brown bear presence we selected areas andoverlaid them into thespeciesdistributionmapOnly thebrownbearoccurrencepointswithinprotectedareaswereselectedforfurther analysis to model the potentially suitable habitats forbrownbearWe removed the unconfirmedbrownbear distribu-tionareas (potentialdistribution)which layoutsideofprotectedareasthroughouttherangeonwhichwedidnothaveevidenceofpresence In thiswaywe validated brownbear presence pointscollectedfromfieldsurveysandfromliteratureandusedthemforfinal analysisWe also created500presence pointswithin eachprotectedarea(onepointper5kmtimes5kmcell)thatoverlaidwiththe IUCNrsquosbrownbeardistributionmapusingHawthrsquos toolsex-tensioninArcGISWeverifiedtherandomlygeneratedpresencepointsbybrownbearexperts fromChinaMongoliaNepal andIndiaWedidfieldverificationofthoserandomlygeneratedpointsin China andNepal by consultingwith local park authorities todetermine the current brownbear presence and removed thosepoints from the analysiswhere absencewas indicatedWe alsoremoved duplicate presence points and retained only one pres-encepointsper1-km2gridscellsAftervalidationverificationofpresencepointsandremovalofduplicatesweusedremaining209occurrencepointsofbrownbearpresenceforfurtheranalysis

22emsp|emspBioclimatic data

Weusednineteenbioclimaticvariablesderivedfromwwwworldclimorg(Hijmansetal2005)landuselandcoverdatafromgloballandcoverdata(httpswwwglcnorgLathametal2014)andaltitudefromGTOPO30 (httpsltacrusgsgovGMTED2010DanielsonampGesch2011)Wepreparedaspectandslope layersusingadigitalelevationmodel(DEM)layerusingArcGISandclippedallvariablestoourstudyareasWethenextractedthevaluesofeachvariablecorrespondingtothespeciesoccurrencelocationstoperformcor-relation analysis and removed highly correlated variables (gt085Table1)Weusedtheremaining14variablesforourfinalanalysis

For projections of future climate we used the MIROC5(Model for Interdisciplinary Research On Climate) GeneralCirculationModel (GCM)developedby theUniversityofTokyoNational Institute for Environmental Studies Japan Agency for

F I G U R E 1 emspBrownbear(Ursus arctos)


Marine-Earth Science and Technology (Sperber et al 2013Sharmila Joseph Sahai Abhilash amp Chattopadhyay 2015Mishra et al 2014) TheGCMdatawere downscaled using thedeltamethod and bias corrected byworldclimrsquos current climate(httpsworldclimorg) We ran the MIROC5 model using theRepresentative Concentration Pathway 45 a ldquomiddle-of the-roadrdquoGHG(GreenHouseGas)scenarioForouranalysisweused

currentand2050 (average for2041ndash2060) timeseriesclimatechangescenario(httpsworldclimorgcmip5_30s)

23emsp|emspModeling current and future suitable habitat

Weusedmaximumentropy(MaxEnt)speciesdistributionmodeling(SDMPhillipsStevenandDudiacutek2008)tomapthecurrentandpre-dictedfuturedistributionofbrownbearinthestudyareaMaxEntis a widely used tool for modeling species distributions usingpresence data of species and various environmental parameters(Kramer-Schadtetal2013)TherearelimitationsinMaxEntmod-eling (Boria Olson Goodman amp Anderson 2014 RadosavljevicampAnderson2013)Weminimizedthese limitationsbyusingvali-dated presence data (from field surveys past studies and IUCNdistributions map) Finally we evaluated and selected the bestmodel projectionof current and future scenarios Sinceour datawere based on field surveys and areaswith existing brown bearpresenceinprotectedareastheremaybesomebiasesduetoauto-correlationoflocalitiesandvariables(Boriaetal2014)thereforewevalidated themodel using the areaunder the curve (AUC)ofthe receiver operator characteristic (ROC) curve to correct forbiasedsamplesandvariables (Pearceetal2000Roura-PascualBrotonsPetersonampThuiller2009)Wepreparedsuitablehabitatof brownbear based on equal training sensitivity and specificitylogistic threshold (Table2)andremovedtheareabelowlt039ofequaltrainingsensitivityandspecificitylogisticthreshold(Table2)

3emsp |emspRESULTS

Afterremovinghighlycorrelatedvariables(gtr=085)weused14variables for further analysis such as Temperature Seasonality(BIO4) Max Temperature of Warmest Month (BIO5) MeanTemperature of Driest Quarter (BIO9) Mean Temperature of

TA B L E 1 emspRelativecontributionofenvironmentvariabletotheMaxEntmodel

VariablesPercent contribution

Permutation importance

AnnualMeanTemperature(BIO1)

439 583

MeanTemperatureofWettestQuarter(BIO8)

271 02

PrecipitationofDriestMonth(BIO14)

52 27

MinTemperatureofColdestMonth(BIO6)

44 22

AnnualPrecipitation(BIO12) 43 17

Elevation 43 73

Aspect 23 17

TemperatureAnnualRange(BIO7)

21 144

Slope 21 08

Landcover 12 1

PrecipitationSeasonality(BIO15)

1 47

MeanDiurnalRange(BIO2) 08 15

Isothermality(BIO3) 07 28

PrecipitationofColdestQuarter(BIO19)

05 07

TA B L E 2 emspCommonthresholds(cumulativeandlogistic)andcorrespondingomissionrates

Cumulative threshold Logistic threshold DescriptionFractional predicted area

Training omission rate

1000 0032 Fixedcumulativevalue1 0629 0000



2652 0067 Minimumtrainingpresence 0519 0000

19020 0280 10percentiletrainingpresence 0226 0099

26635 0363 Equaltrainingsensitivityandspecificity 0173 0171

19871 0292 Maximumtrainingsensitivityplusspecificity 0218 0105

2652 0067 Balancetrainingomissionpredictedareaandthresholdvalue

0519 0000

9876 0170 Equateentropyofthresholdedandoriginaldistributions

0334 0046

NoteIftestdataareavailablebinomialprobabilitiesarecalculatedexactlyifthenumberoftestsamplesisatmost25otherwiseusinganormalap-proximationtothebinomialTheldquoBalancerdquothresholdminimizes6timestrainingomissionrate+004timescumulativethreshold+16timesfractionalpredictedarea


WarmestQuarter(BIO10)MeanTemperatureofColdestQuarter(BIO11) Precipitation of Wettest Month (BIO13) Precipitationof Wettest Quarter (BIO16) Precipitation of Warmest Quarter(BIO18)andPrecipitationofDriestQuarter (BIO17 (SupportinginformationTableS1)Overall annual and seasonal temperatureand precipitationwere themain bioclimatic factors contributingtobrownbearhabitatsuitabilitywhichtogethercontributedmorethan90tothespeciesdistributionmodel(Table1)AnnualMeanTemperature (BIO1) contributed the most (439) followed byMeanTemperatureofWettestQuarter(BIO8271)PrecipitationofDriestMonth(BIO1452)MinimumTemperatureofColdestMonth (BIO1144)andAnnualPrecipitation (BIO1243) tothemodelAspectslopeandlandcovercontributedlt3toourmodel(Table1)

Theresultof the jackknife testofvariable importanceshowedthat highest gain was in annual mean temperature and elevation(Figure 2) The environmental variable which decreased the gain

themostwhen itwasomittedwas the landcover (Figure2)Ourmodelwaswell represented because the omission ratewas closetothepredictedomissionasafunctionofthecumulativethresholdand bothwere calculated based on the training presence records(Figure3Table2)Ourmodelandenvironmentalvariablesdescribedthecurrentdistributionofbrownbearverywell in thestudyarea(AUC=090Figures2‒4)Responsecurvesshowedeachenviron-mentalvariableaffectedthepredictionofbrownbeardistributionwhichkeepsallotherenvironmentalvariablesattheiraveragesam-plevalueandshowedhowthe logisticpredictionchangesaseachenvironmentalvariableisvaried(Figure5)

31emsp|emspRole of temperature and precipitation on brown bear habitat

Ourmodel showed that brown bear distributionwas attributedto bioclimatic variables associated with climate change annual

F I G U R E 2 emspResultsofthejackknifetestofvariableimportanceTheenvironmentalvariablewithhighestgainwhenusedinisolationisMeanTemperatureofWarmestQuarter(Bio10)whichthereforeappearstoprovidethemostusefulinformationbyitselfTheenvironmentalvariablethatdecreasesthegainthemostwhenomittedislandcoverwhichappearstohavethemostinformationthatisntpresentintheothervariables

TA B L E 3 emspCurrentandfuturesuitablehabitatofbrownbear

CountryCurrent suitable habitat (area in km2) Current area in

Future (2050) suitable habitat (area in km2) of Change

Mongolia 47750300 1387 46588000 minus243

Afghanistan 4747470 138 4240230 minus1068

Kazakhstan 17632000 512 16071100 minus885

Tajikistan 7615390 221 7521530 minus123

Kyrgyzstan 11876800 345 11164100 minus600

Uzbekistan 1027170 030 1552340 5113

China 225981000 6566 196961000 minus1284

India 14100200 410 10388200 minus2633

Bhutan 1418210 041 1308400 minus774

Nepal 4050590 118 3513230 minus1327

Pakistan 6850260 199 5650130 minus1752

Total 343049390 305163260 minus1104


temperature (BIO1) andprecipitation (BIO12 Table 1) The spa-tially averaged currentmean annual temperature of brownbearhabitat was minus12degC (maximum 171 minimum minus137degC) and ispredicted to increase to 16degC (maximum 199degC and minimumminus112degC)by2050Similarlycurrentannualmeanprecipitationofbrownbearhabitatispredictedtoincreaseby13from406mmto459mmby2050

32emsp|emspSuitable habitats of brown bear under current and future climates

Ourmodel showed that present suitable brownbear habitat areawas343049390km2inCentralAsia(Figure6)MostofthehabitatslocatedinChina(657)followedbyMongolia(139)Kazakhstan(51)India(41)Kyrgyzstan(35)andPakistan(20Table3Figure6)TheleastamountofsuitablehabitatwasfoundinBhutan

(04) Uzbekistan (03) Nepal (12) and Afghanistan (14Table3Figure6)

Our results showed that the current suitable habitatwill be re-ducedby11 (378861km2) acrossCentralAsiaby2050 (Table3)due toclimatechangeThemost suitablehabitat ispredicted tobelost in India (26 loss) Pakistan (17) and Nepal (13) In China290200km2(13)ofsuitablehabitatispredictedtobelostby2050(Table3)HoweverasmallincreaseinsuitablehabitatforbrownbearispredictedinUzbekistanrelativetotheentirestudyarea(10271km2)butarelativelylargegainwithinthecountry(51Table3Figure6)

33emsp|emspSuitable habitat within protected areas

About 18 of the areas from the current total suitable habitatlay within protected areas (1124330km2) which is predicted todecrease to 1103912km2 by 2050 (Table 4) In some countries

F I G U R E 3 emspTheomissionrateandpredictedareaasafunctionofthecumulativethresholdTheomissionrateiscalculatedbothonthetrainingpresencerecordsand(iftestdataareused)onthetestrecordsTheomissionrateshouldbeclosetothepredictedomissionbecauseofthedefinitionofthecumulativethreshold

F I G U R E 4 emspThereceiveroperatingcharacteristic(ROC)curveforthesamedataNotethatthespecificityisdefinedusingpredictedarearatherthantruecommissionThisimpliesthatthemaximumachievableAUCislessthan1IftestdataaredrawnfromtheMaxEntdistributionitselfthenthemaximumpossibletestAUCwouldbe0868ratherthan1inpracticethetestAUCmayexceedthisbound


however suitable habitat losswithin protected areaswas greaterForexampleIndiawillexperiencethegreatestlossat27ofsuit-able habitats followed by Tajikistan (68 loss) Chinarsquos predictedlosswithinprotectedareasisabout12841km2(14)ofasuitableareaby2050Howeversuitablehabitatwithinprotectedareas ispredictedto increase insomecountriessuchasUzbekistan (21)andBhutan(9Table4)

4emsp |emspDISCUSSION

Habitat use by organisms reflects the environmental characteris-ticsthataugmenttheirfitness(Fretwell1969)Generallyitissup-posedthataspeciesdistributionorindividualswithinapopulationis a good indicator of habitat structure and particularlymanifeststheir preference toward the habitat qualities Predictivemodeling

F I G U R E 5 emspResponsecurvesThesecurvesshowhoweachenvironmentalvariableaffectstheMaxEntpredictionThecurvesshowhowthelogisticpredictionchangesaseachenvironmentalvariableisvariedkeepingallotherenvironmentalvariablesattheiraveragesamplevalue


hasbecomeavaluabletoolforsuccessfulconservationplanningorwildlifemanagementthroughidentificationandpredictionofhabitatappropriatenessforgivenspecies(Schadtetal2002)Indeedpre-dicting futuregeographical rangebyspeciesdistributionmodelingispivotaltounderstandtheirecologicalrequirementsandbiologicalresponses toupcomingclimaticchanges(DuanKongHuangFanampWang2014)

Across Central Asia suitable habitats of the brown bear arewidelydistributed inhigherelevationregionsandarepredictedtomoderatelydecreaseby2050duetoclimatechangehowevertheextentof thechange isnot feltequally in thecountries InChinawheremostofthecurrentsuitablehabitatforbrownbearsisfoundalossof13ofsuitablehabitatislikelytohaveasignificantimpactonthedistributionofbearsinthecountrybutmuchofthischangewilloccuroutside theprotectedareaswithaminorchange in thehabitatsinsideprotectedareasForcountrieswhichhavesmallsuit-ableareasforbrownbearslossofsuitablehabitatmayhavemore

profoundeffectsIndiaforexamplewhichoffersarelativelysmallamountofsuitablehabitat forbrownbears is likelytoexperiencethegreatestimpactonbrownbeardistributiongiventhesignificantlossofpredictedhabitatsinsideprotectedareasAsimilarsituationwasobservedinPakistanandNepalThereforetheestablishmentof future protected areas may be necessary to ensure that theextirpation of bears does not occur in these areas such as IndiaPakistanandNepalWhilesuitablehabitatispredictedtoincreaseinUzbekistanandBhutansuchanincreaseisunlikelytooffsetthetotallossofhabitattobrownbearsinCentralAsiaasthosecountrieshaveverylittlesuitablebrownbearhabitat(Aryaletal2014)Anadaptiveapproach toestablish futureprotectedareas in responsetoclimate-inducedchangeisnecessarytoensurethepersistenceofthespeciesinthisregion

Wehypothesizethattwobioclimaticvariablesannualprecipita-tionandtemperaturemaysignificantlychallengethegeographicaldistributionofbrownbears inCentralAsiabypotentialdirectand

F I G U R E 6 emspCurrentandfuturesuitablehabitatofbrownbearinAsia


indirecteffectsTheseeffectsarenotonlyanticipatedtocauseshiftsinbrownbeardistributionsasspeciesoftenpursueanoptimalhab-itatbutthreateningtheirviabilityduetorangereductionsorfrag-mentationsandpartiallyalteringtheirbiologicalsystems(Parmesan2006)Ourresultshighlightedtheinfluenceoffuturemeteorologicalconditions on behavioral plasticity the ability to respond to envi-ronmental changes which will dictate howwell brown bears canadjustorresisttochangesoccurringintheirenvironment(WilliamsShooIsaacHoffmannampLangham)Forexamplebrownbearstendtomodify their ambulatoryactivitiesandmovement speedduringperiodsofincreasedprecipitationwithanincreaseof01kmhrforeachincreaseof5mmofrainfall(Martin2009)whichmightpredicttherelativelygreaterenergeticcostsoffuturehigh-speedlocomo-tionofbrownbearstomeettheirbasicrequirements(GormezanoMcWilliamsIlesampRockwell2016)bytheprobableincreaseinpre-cipitation from406 to459mmby2050Similarly thepredicatedhighprecipitation should accelerate themeltingof snow increasetherun-offandcausestreamstooverflowOnonehandthiscouldreducetheperiodduringwhichsnowstilloffersaprotectiveshelterforoptimaldenningstructureandenvironmentOntheotherhanddue topoorwinterprecipitation the snowdepthand snowcoverinalpinescrubandmeadowhabitatswouldbeverylessleadingtochanges in plant community structure composition and biomassinthefollowingspringandsummerThiscouldforceindividualstomovemore in search of better quality habitats increasing energycosts Furthermore disturbances resulting in displacement at thisstageof the lifecyclecouldhavedeleteriouseffectsespecially inthepresenceofaltricialbearcubsdevelopinglocomotoryskillsasanewdensitemustbefoundandtheoffspringneedtoberelocated(JohnSwensonAndersenampBarnes2000)

Our results also highlighted the influence of predicted tem-perature increase from minus12degC to 16degC by 2050 on brown bearThe global change in temperaturewill inevitably lead to challeng-ing impactsnotonlyonbrownbeardistributionpatternsbutalsoon their ethological repertoireandcyclic and seasonal changesof

biological activities Generallymammals can copewith escalatingthermal stress by adopting some thermoregulatorybehavioralre-sponses(Sawaya Ramsey amp Ramsey 2017)including shifting tomorenocturnalactivitiesasaleast-costthermoregulationstrategytoreducethecostsassociatedwithautonomictemperatureregula-tion(MaloneyMossCartmellampMitchell2005)Bearsarelargelydiurnal(MacHutchon 2001)but become less active at daytimeandmorenocturnalwhentemperaturerises(McLellanampMcLellan2015)Similarlyfailureorinadequacyofthebehavioralthermoreg-ulatorymeasureswillinevitablyleadtocostlierphysiologicaladap-tations to climate changes For instance increased temperatureshave been strongly linked to shorter periods of denning in bears(InouyeBarrArmitageampInouye2000)Shorterdurationsofhiber-nationscouldleadtoalteredenergybudgetsreducedcubsurvivaland fitness and higher incidents of humanndashbear conflicts (PigeonStenhouseampCocircteacute2016)Finallyanexaminationofregionalstud-ies over a 50-year period showed that carnivore body sizes havegenerallyincreasedoverthepasthalf-centuryThismaybearesultfrom the increases in the length ofwarm season associatedwithclimatechange(Yom-Tov2003)Followingthistrendbrownbearsmayalsoincreaseintheirbodysizethatmandatesextra-energyde-mandswhich could threat the predatorndashprey relationship throughmagnifying predation effects and reduce the probability of preycoexistence(ThakurKunneGriffinampEisenhauer2017)Anexam-plecouldalsoclarifytheeffectofclimatechangeonpredatorndashpreydynamics in the region(Aryal et al 2014) Brown bears can preyheavilyonsmallmammalssuchaspika(Ochotonaspp)andmarmot(Marmota spp)athighaltitudeswhicharesensitivetotemperatureand precipitation changes(Francl Hayhoe Saunders amp Maurer2010)thereforefutureclimatechangemayaltertheirdistributionandpopulationdynamicsPikaandmarmotwhicheffectivelyinhabithigh-elevationldquoislandsrdquomayhavetomigrateupwardsinelevationinordertoliveunderpreferredclimateconditionsIfclimatechangescausereductionsinwildpreypopulationsoravailabilitytheremaybeanincreasedriskofbrownbearsswitchingtheirfeedingstrategy

TA B L E 4 emspSuitablehabitatwithinprotectedareascurrentandprojectedfor2050

CountryCurrent suitable habitat within protected area (area in km2)

Future (2050) suitable habitat within protected area (area in km2) of Change

Mongolia 6052740 6270320 359

Afghanistan 629029 592230 minus585

Kazakhstan 1624750 1618160 minus041

Tajikistan 2457960 2289790 minus684

Kyrgyzstan 599036 579669 minus323

Uzbekistan 527812 640147 2128

China 94067200 92783100 minus137

India 3312480 2416220 minus2706

Bhutan 557279 611163 967

Nepal 1873680 1859730 minus074

Pakistan 731058 730727 minus005

Total 112433024 110391256 minus182


tokillmorelivestockintheregion(Aryaletal20122010)therebyexacerbatinghumanndashbearconflict

Any lossof suitablehabitatwithinprotectedareas isofcon-cernforbrownbearconservationinCentralAsiabecauseitmayresult in bears moving out of protected area due to climate-in-ducedrangeshift (Upwardandnorthward)Suchmovementmayincrease encounters with humans and a subsequent increase inhumanndashbear conflicts and increased bear mortalities Howevermore research is necessary to determine the impact of climatechange on food resources (bottom-up regulation) and nutritionof bears As well the addition of mortality risk to bear modelswill help tounderstand top-down factors thatmayaffectpopu-lations(NielsenMcDermidStenhouseampBoyce2010)Thedatanecessary to resolve such nutritional and mortality-related fac-torsaretoourknowledgenotavailableacrosstheentiretyofourimmensestudyareasbutshouldbeafocusoffutureresearchInaddition toupwardsmigration futureclimatechangemaycausesomemammalspeciestomovenorthward(Francletal2010)Therange shift from southern areas such as IndiaNepal andChinato northern regions such asMongolia would be unlikely due tohabitatfragmentationandloss(Inkleyetal2004Rosenzweigetal2008)Suchasituationmightcontributetolocalextirpationofbrownbearand lowgeneticdiversity(Guralnick2006Hadlyetal 2004)Toprevent thisbrownbearmovementbetweensuit-able habitats should be facilitated through the development ofcorridorswhichconnecthabitatbetweenprotectedareas indif-ferent countries (Ramiadantsoa Ovaskainen Rybicki amp Hanski2015)Suchaconservationeffortwouldofcoursebechalleng-ing and require the participation and collaboration of differentcountries

ACKNOWLEDG MENTS

This work was supported by the National Natural ScienceFoundationofChinaunderGrant(31460566and31760706)GansuProvincial Natural Science Foundation forDistinguishedYoungScholarsof China under Grant (1606RJDA314) the InternationalCooperationResearchProgrammeofMasseyUniversityResearchFundunderGrant[GAMU-RCGB-1401]ldquoFuxiTalentrdquoPlanofGansuAgriculturalUniversityunderGrant[Gaufx-02J03]SpecialfundsfordisciplineconstructionofGansuAgriculturalUniversityunderGrant[GSAU-XKJS-2018-003]theAlertisFundforNatureConservationNetherlands and Talented Young Scientists fellowship (TYSP) oftheMinistryofScienceandTechnologyofChina for fundingsup-port Weare thankful to the Steppe Forward Programme (SFP)ofMongolia andMongolianAcademyof Sciences (MAS) for shar-ingpresencedataofbrownbear

FieldsurveyswereapprovedbyethicalcommitteesofMasseyUniversity Alertis Fund for Nature Conservation MongolianAcademy of Sciences Gansu Agricultural University and localauthoritieswherethefieldobservationswereconductedinrele-vantcountriesTheauthorsdeclarethattheyhavenocompetinginterests

AUTHOR CONTRIBUTIONS

JSUBSSCCSSMDZDYSXDHGFandLWcollectedthedataJSandAAanalyzedthedatadesignedthestudyandsupervisedtheprojectJSIMHUBSSCCSSMDZDYSXDHGFLWandWJparticipatedinthemanuscriptwriting

DATA ACCE SSIBILIT Y

Bioclimaticdataareavailablefordownloadatthedatabaseswwwworldclimorghttpswwwglcnorg and httpsltacrusgsgovGMTED2010Brownbearpresencedatawereuploadedasonline(DataS1)

ORCID

Junhu Su httpsorcidorg0000-0002-3416-6354

Achyut Aryal httporcidorg0000-0001-6658-8714

Weihong Ji httporcidorg0000-0001-5240-3344

R E FE R E N C E S

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AryalA(2012)BrownbearconservationactionplaninNepalEffortschallengesandachievementsWorld Journal of Zoology775ndash78

Aryal A Brunton D amp Raubenheimer D (2014) Impact of climatechange on human-wildlife-ecosystem interactions in the Trans-Himalaya regionofNepalTheoretical and Applied Climatology115517ndash529httpsdoiorg101007s00704-013-0902-4

Aryal A Iii J B H Raubenheimer D JiW amp Brunton D (2012)Distributionanddietofbrownbears in theuppermustangregionnepalUrsus23231ndash236

AryalARaubenheimerDSathyakumarSPoudelBSJiWKunwarKJhellipBruntonD(2012)Conservationstrategyforbrownbearanditshabitat inNepalDiversity4301ndash317httpsdoiorg103390d4030301

AryalASathyakumarSampSchwartzCC (2010)Current statusofbrown bears in themanasalu conservation area NepalUrsus21109ndash114httpsdoiorg10219209GR0291

BellardCBertelsmeierCLeadleyPThuillerWampCourchampF(2012)ImpactsofclimatechangeonthefutureofbiodiversityEcologyLetters15365ndash377httpsdoiorg101111j1461-0248201101736x

BertelsmeierCLuqueGMampCourchampF(2013)Increaseinquantityandqualityofsuitableareasfor invasivespeciesasclimatechangesConservation Biology the Journal of the Society for Conservation Biology271458ndash1467httpsdoiorg101111cobi12093

BoriaRAOlsonLEGoodmanSMampAndersonRP(2014)Spatialfiltering to reduce sampling bias can improve the performance ofecologicalnichemodelsEcological Modelling27573ndash77httpsdoiorg101016jecolmodel201312012

ChenICHillJKOhlemullerRRoyDBampThomasCD(2011)Rapid range shifts of species associated with high levels of cli-mate warming Science 333 1024ndash1026 httpsdoiorg101126science1206432

ChenYLiWDengHFangGampLiZ (2016)Changes inCentralAsiasWaterTowerPastPresentandFutureScientific Reports635458


CraneTARoncoliCampHoogenboomG(2011)AdaptationtoclimatechangeandclimatevariabilityTheimportanceofunderstandingag-ricultureasperformanceNJAS ‐ Wageningen Journal of Life Sciences57179ndash185httpsdoiorg101016jnjas201011002

Danielson J JampGeschDB (2011)GlobalMulti-resolutionTerrainElevationData2010GMTED2010USGeo-SurveySurveyOpen-FileReport2011ndash107326

DuanRYKongXQHuangMYFanWYampWangZG(2014)Thepredictiveperformanceandstabilityofsixspeciesdistributionmodels PLoS One 9 e112764 httpsdoiorg101371journalpone0112764

EttersonJRampMazerSJ(2016)ECOLOGYHowclimatechangeaf-fectsplantssexlivesScience35332ndash33httpsdoiorg101126scienceaag1624

FranclKEHayhoeKSaundersMampMaurerEP(2010)EcosystemadaptationtoclimatechangeSmallmammalmigrationpathwaysintheGreatLakes states Journal of Great Lakes Research36 86ndash93httpsdoiorg101016jjglr200909007

FretwellSD(1969)Onterritorialbehaviorandotherfactorsinfluenc-inghabitatdistributioninbirdsActa Biotheoretica1945ndash52httpsdoiorg101007BF01601955

GarciaRACabezaMRahbekCampAraujoMB (2014)Multipledimensions of climate change and their implications for biodi-versity Science 344(6183) 1247579 httpsdoiorg101126science1247579

GongJampHarrisR(2006)ThestatusofbearsinChinaInJapanBearNetwork (Ed)Understanding Asian bears to secure their future (pp96ndash101)IbarakiJapanJapanBearNetwork

GormezanoLJMcWilliamsSRIlesDTampRockwellRF(2016)CostsofLocomotioninPolarBearswhendotheCostsOutweightheBenefitsofChasingdownTerrestrialpreyConservation Physiology4cow045httpsdoiorg101093conphyscow045

GuralnickR (2006)The legacyofpastclimateand landscapechangeonspeciesrsquocurrentexperiencedclimateandelevationrangesacrosslatitude Amultispecies study utilizingmammals inwesternNorthAmericaGlobal Ecology and Biogeography15505ndash518httpsdoiorg101111j1466-822X200600231x

HadlyEARamakrishnanUChanYLvanTuinenMOKeefeKSpaethPAampConroyC J (2004)Genetic response to climaticchange Insights from ancient DNA and phylochronology PLoS Biology2e290httpsdoiorg101371journalpbio0020290

HijmansRobert JCameronSusanEParra JuanL JonesPeterGamp Jarvis A (2005) Very high resolution interpolated climate sur-faces for global land areas International Journal of Climatology251965ndash1978

Hill J K Griffiths H M amp Thomas C D (2011) Climate changeand evolutionary adaptations at species range margins Annual Review of Entomology 56 143ndash159 httpsdoiorg101146annurev-ento-120709-144746

HoffmannAAampSgroCM (2011)Climate changeandevolution-ary adaptation Nature 470 479ndash485 httpsdoiorg101038nature09670

HulmePE(2016)ClimatechangeandbiologicalinvasionsEvidenceex-pectationsandresponseoptionsBiological Reviews of the Cambridge Philosophical Society 92(3) 1297ndash1313 httpsdoiorg101111brv12282

Inkley D B AndersonM G Blaustein A R Burkett V R FelzerBGriffithBhellipRootTL (2004)Global climate change and wild‐life in North America Wildlife Society Technical Review 04ndash2 (p 26)BethesdaMarylandTheWildlifeSociety

Inouye D W Barr B Armitage K B amp Inouye B D (2000)Climate change is affecting altitudinal migrants and hibernatingspecies Proceedings of the National Academy of Sciences of the United States of America971630ndash1633httpsdoiorg101073pnas9741630

IUCNandUNEP-WCMC(2014)The World Database on Protected Areas WDPA[On-line]CambridgeUKUNEP-WCMCAvailableatwwwprotectedplanetnet

IUCNandWildlifeConservationSociety(2008)UrsusarctosTheIUCNRedlistofThreatenedspeciesVersion20143

JerinaKJonozovicMKrofelMampSkrbinsekT (2013)Rangeandlocal population densities of brown bearUrsus arctos in SloveniaEuropean Journal of Wildlife Research 59 459ndash467 httpsdoiorg101007s10344-013-0690-2

JohnDSwensonJAndersenRampBarnesB(2000)HowVulnerableAreDenningBears toDisturbanceWildlife Society Bulletin1973ndash2006(28)400ndash413

Kramer-Schadt S Niedballa J Pilgrim John D Schroumlder BLindenbornJReinfelderVampRobertsonM(2013)Theimpor-tanceofcorrecting forsamplingbias inMaxEntspeciesdistribu-tionmodelsDiversity and Distributions191366ndash1379httpsdoiorg101111ddi12096

KujalaHMoilanenAAraujoMBampCabezaM(2013)Conservationplanning with uncertain climate change projections PLoS One 8e53315httpsdoiorg101371journalpone0053315

LathamJCumaniRRosatiIampBloiseM(2014)GlobalLandCoverSHAREGLC-SHAREdatabaseBeta-V10ndash2014Technicalreport

LoarieSRCarterBEHayhoeKMcMahonSMoeRKnightCAampAckerlyDD(2008)ClimatechangeandthefutureofCaliforniasendemicfloraPLoS One3e2502httpsdoiorg101371journalpone0002502

LoginovD(2012)InternationalBearNewsQuarterlyNewsletteroftheInternationalAssociation forBearResearchandManagement IBAandtheIUCNSSCBearSpecialistGroup211

LordJampWhitlatchR(2015)Predictingcompetitiveshiftsandresponsestoclimatechangebasedonlatitudinaldistributionsofspeciesassem-blagesEcology961264ndash1274httpsdoiorg10189014-04031

LundhedeTHJacobsenJBHanleyNFjeldsaJRahbekCStrangeNampThorsenBJ(2014)Publicsupportforconservingbirdspeciesruns counter to climate change impacts on their distributionsPLoS One9e101281httpsdoiorg101371journalpone0101281

MacHutchonAG(2001)GrizzlyBearActivityBudgetandPatternintheFirthRiverValleyYukonUrsus12189ndash198

MaloneySKMossGCartmellTampMitchellD (2005)Alterationindielactivitypatternsasathermoregulatorystrategyinblackwil-debeest (Connochaetes gnou) Journal of Comparative Physiology A Neuroethology Sensory Neural and Behavioral Physiology1911055ndash1064httpsdoiorg101007s00359-005-0030-4

Martin J (2009)Habitat selection andmovement by brown bears inmultiple-use landscapesDoctoral thesisNorwegianUniversity ofLifeSciencesAringsandUniversiteacuteClaudeBernardndashLyon1UniversiteacutedeLyonLyon

MccarthyTMWaitsLPampMijiddorjB (2014)Statusof thegobibear in mongolia as determined by noninvasive genetic methodsUrsus2030ndash38

McLellanBNServheenCampHuberD(2008)UrsusarctosInIUCN2013IUCNRedListofThreatenedSpeciesVersion20132[wwwiucnredlistorg]

McLellanMLampMcLellanBN(2015)Effectofseasonandhighambi-enttemperatureonactivitylevelsandpatternsofgrizzlybears(Ursus arctos) PLoS One 10 e0117734 httpsdoiorg101371journalpone0117734

MishraVKumarDGangulyARSanjayJMujumdarMKrishnanR amp Shah R D (2014) Reliability of regional and global climatemodels to simulate precipitation extremes over India Journal of Geophysical Research‐Atmospheres 119 9301ndash9323 httpsdoiorg1010022014JD021636

MohebZLawsonDampMostafawiSN(2012)Brownbearstatusandthreats in Darwaz Northern Badakhshan Afghanistan Ursus 23237ndash240httpsdoiorg102192URSUS-D-12-000011


MunozARMarquezALampRealR(2015)Anapproachtoconsiderbehavioral plasticity as a source of uncertainty when forecastingspeciesresponsetoclimatechangeEcology and Evolution52359ndash2373httpsdoiorg101002ece31519

Nawaz M A (2007) Status of the Brown Bear in Pakistan Ursus18 89ndash100 httpsdoiorg1021921537-6176(2007)18[89SOTBBI]20CO2

NawazMASwensonJEampZakariaV (2008)Pragmaticmanage-ment increases a flagship species the Himalayan brown bears inPakistanrsquosDeosaiNationalParkBiological Conservation1412230ndash2241httpsdoiorg101016jbiocon200806012

NielsenSEMcDermidG StenhouseGBampBoyceMS (2010)DynamicwildlifehabitatmodelsSeasonalfoodsandmortalityriskpredictoccupancy-abundanceandhabitatselectioningrizzlybearsBiological Conservation143 1623ndash1634 httpsdoiorg101016jbiocon201004007

Parmesan C (2006) Ecological and Evolutionary Responses toRecent Climate Change Annual Review of Ecology Evolution and Systematics 37 637ndash669 httpsdoiorg101146annurevecolsys37091305110100

PearceJampFerrierS(2000)EvaluatingthepredictiveperformanceofhabitatmodelsdevelopedusinglogisticregressionEcological Modelling133225ndash245httpsdoiorg101016S0304-3800(00)00322-7

Phillips Steven J amp Dudiacutek M (2008) Modeling of species dis-tributions with Maxent New extensions and a compre-hensive evaluation Ecography 31 161ndash175 httpsdoiorg101111j0906-759020085203x

PigeonK E StenhouseGampCocircteacute SD (2016)Drivers of hiberna-tionLinkingfoodandweathertodenningbehaviourofgrizzlybearsBehavioral Ecology and Sociobiology 70 1745ndash1754 httpsdoiorg101007s00265-016-2180-5

Pound M J amp Salzmann U (2017) Heterogeneity in global vege-tation and terrestrial climate change during the late Eocene toearlyOligocene transitionScientific Reports7 43386 httpsdoiorg101038srep43386

PresseyRLCabezaMWattsMECowlingRMampWilsonKA(2007)ConservationplanninginachangingworldTrends in Ecology amp Evolution22583ndash592httpsdoiorg101016jtree200710001

RadosavljevicAampAndersonRP (2013)Makingbettermaxentmo-dels of species distributions Complexity overfitting and evalua-tionJournal of Biogeography41629ndash643httpsdoiorg101111jbi12227

RamiadantsoaTOvaskainenORybickiJampHanskiI(2015)Large-Scalehabitatcorridorsforbiodiversityconservationaforestcorridorin Madagascar PLoS One 10 e0132126 httpsdoiorg101371journalpone0132126

RobertsD RNielsen S Eamp StenhouseG B (2014) Idiosyncraticresponses of grizzly bear habitat to climate change based on pro-jectedfoodresourcechangesEcological Applications A Publication of the Ecological Society of America 24 1144ndash1154 httpsdoiorg10189013-08291

RosenzweigCKarolyDVicarelliMNeofotisPWuQCasassaGhellipImesonA(2008)AttributingphysicalandbiologicalimpactstoanthropogenicclimatechangeNature453353ndash357httpsdoiorg101038nature06937

Roura-Pascual N Brotons L Peterson A T amp ThuillerW (2009)Consensualpredictionsofpotentialdistributionalareasforinvasivespecies A case study of Argentine ants in the Iberian PeninsulaBiological Invasions 11 1017ndash1031 httpsdoiorg101007s10530-008-9313-3

SathyakumarS(2001)StatusandmanagementofAsiaticblackbearandHimalayanbrownbearinIndiaUrsus1221ndash29

SathyakumarS(2006)StatusanddistributionofHimalayanbrownbearUrsus arctos isabellinusinIndiaAnassessmentofchangesovertenyearsInd for13289ndash96

Sathyakumar S Kaul R AshrafN KMookherjee A ampMenon V(2012)National bear conservation and welfare action plan (p 359)MinistryofEnvironmentandForestsWildlifeInstituteofIndiaandWildlifeTrustofIndia

SawayaMARamseyABampRamseyPW (2017)AmericanblackbearthermoregulationatnaturalandartificialwatersourcesUrsus27129ndash135httpsdoiorg102192URSU-D-16-000101

Schadt S Knauer F Kaczensky P Revilla E WiegandT amp Trepl L (2002) Rule-based assessment of suit-able habitat and patch connectivity for the eurasianlynx Ecological Applications 12 1469ndash1483 httpsdoiorg1018901051-0761(2002)012[1469RBAOSH]20CO2

SeimAOmurovaGAzisovEMusuralievKAlievKTulyaganovThellipLinderholmHW (2016)ClimateChange IncreasesDroughtStressofJuniperTreesintheMountainsofCentralAsiaPLoS One11e0153888httpsdoiorg101371journalpone0153888

SharmilaS JosephSSahaiAKAbhilashSampChattopadhyayR(2015) Future projection of Indian summer monsoon variabilityunder climate change scenario An assessment from CMIP5 cli-matemodelsGlobal and Planetary Change124 62ndash78httpsdoiorg101016jgloplacha201411004

ShresthaUBampBawaKS (2014) Impactofclimatechangeonpo-tential distribution of Chinese caterpillar fungus (Ophiocordyceps sinensis) in Nepal Himalaya PLoS One 9 e106405 httpsdoiorg101371journalpone0106405

ShresthaUBGautamSampBawaKS (2012)WidespreadclimatechangeintheHimalayasandassociatedchangesinlocalecosystemsPLoS One7e36741httpsdoiorg101371journalpone0036741

SodhiNSKohLPBrookBWampNgPK(2004)SoutheastAsianbiodiversityAnimpendingdisasterTrends in Ecology amp Evolution19654ndash660httpsdoiorg101016jtree200409006

SperberKAnnamalaiHKang I SKitohAMoiseATurnerAhellip Zhou T (2013) The Asian summer monsoon An intercom-parison of CMIP5 vs CMIP3 simulations of the late 20th cen-tury Climate Dynamics 41 2711ndash2744 httpsdoiorg101007s00382-012-1607-6

Su JH Aryal A ANan Z B amp JiWH (2015) Climate change-inducedrangeexpansionofasubterraneanrodentImplicationsforrangeland management in Qinghai-Tibetan Plateau PLoS One 10e0138969httpsdoiorg101371journalpone0138969

ThakurMPKunneTGriffinJNampEisenhauerN(2017)Warmingmagnifiespredationandreducespreycoexistenceinamodel litterarthropod system Proceedings Biological Sciences 284 20162570httpsdoiorg101098rspb20162570

Torres-DiazCGallardo-CerdaJLavinPOsesRCarrasco-UrraFAtalaChellipMolina-MontenegroMA(2016)BiologicalInteractionsand Simulated Climate Change Modulates the EcophysiologicalPerformanceofColobanthusquitensis in theAntarcticEcosystemPLoS One 11 e0164844 httpsdoiorg101371journalpone0164844

WaltherGRPostEConveyPMenzelAParmesanCBeebeeT J hellip Bairlein F (2002) Ecological responses to recent climatechangeNature416389ndash395httpsdoiorg101038416389a

WikelskiMampTertitskiG(2016)ECOLOGYLivingsentinelsforclimatechangeeffectsScience352775ndash776httpsdoiorg101126sci-enceaaf6544

WuJ(2016)DetectingandAttributingtheEffectsofClimateChangeon the Distributions of Snake Species Over the Past 50 YearsEnvironmental Management57207ndash219

WuXLuYZhouSChenLampXuB(2016)ImpactofclimatechangeonhumaninfectiousdiseasesEmpiricalevidenceandhumanadapta-tionEnvironment International8614ndash23httpsdoiorg101016jenvint201509007

Xu J amp Grumbine R E (2014) Integrating local hybrid knowledgeand state support for climate change adaptation in the Asian


Highlands Climatic Change 124 93ndash104 httpsdoiorg101007s10584-014-1090-7

Xu JGrumbine R E Shrestha A ErikssonM Yang XWang YampWilkes A (2009) Themelting Himalayas Cascading effects ofclimatechangeonwaterbiodiversityandlivelihoodsConservation Biology the Journal of the Society for Conservation Biology23520ndash530httpsdoiorg101111j1523-1739200901237x

XuACJiangZGLiCWampCaiP(2010)FoodhabitsandhuntingpatternsofTibetanbrownbearduringwarmseasonsinKekexilire-giononQinghai-TibetanPlateauZoological Research31670ndash674

Yom-Tov Y (2003) Body sizes of carnivores commensalwith humanshave increased over the past 50 years Functional Ecology 17323ndash327

YuHLuedelingEampXuJ(2010)WinterandspringwarmingresultindelayedspringphenologyontheTibetanPlateauProceedings of the National Academy of Sciences of the United States of America10722151ndash22156httpsdoiorg101073pnas1012490107

Zhang H X Zhang M L amp Sanderson S C (2013) Retreating orstandingResponsesofforestspeciesandsteppespeciestoclimate

changeinaridEasternCentralAsiaPLoS One8e61954httpsdoiorg101371journalpone0061954

SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle

How to cite this articleSuJAryalAHegabIMetalDecreasingbrownbear(Ursus arctos)habitatduetoclimatechangeinCentralAsiaandtheAsianHighlandsEcol Evol 2018811887ndash11899 httpsdoiorg101002ece34645


1emsp |emspINTRODUC TION

Around the world climate change has had significant direct andindirect impacts on terrestrial species by being amajor cause ofspeciationandspeciesextirpation(PoundampSalzmann2017)Manystudieshaverecentlyfocusedontheecological(EttersonampMazer2016WikelskiampTertitski2016)ethological (MunozMarquezampReal2015)andbiologicalchanges(Torres-Diazetal2016Hulme2016) in relation to climatic change For example various ecosys-tems are vulnerable to climate changewhichmay induce a broadarrayofadverseeffectssuchasdisturbancesofphenologicaleventsfoodwebdisruptionspathogensanddiseasespreadandultimatelyinworstcasescenariosmayincludeextinctionrisks(WuLuZhouChenampXu2016)Furthermoreclimatechangehasimpactedspe-cies distributions by reducing and fragmenting of the area of ani-malhabitats(ChenHillOhlemullerRoyampThomas2011Loarieetal2008LordampWhitlatch2015Lundhedeetal2014SuAryalNanampJi2015Wu2016)Howevertotacklethechallengeofthechangingclimaticconditionsspecieshaveadopteddifferentmech-anisms to counteract themagnitude and speed of climate changeeitherindividuallyorwithinapopulation(HillGriffithsampThomas2011)Forexamplenaturalpopulationsmayreacttoclimatechangeeithercollectivelybyshiftingtheirgeographicalhabitats(Hoffmannamp Sgro 2011) or individually by adjusting their behavioral activi-tiesthroughmodificationsoftheirdietactivityandenergybudgetandreproductivetactics(BellardBertelsmeierLeadleyThuillerampCourchamp2012)Althoughthesetacticalresponseshaveprovento have a short-term efficiency (Crane Roncoli amp Hoogenboom2011)towithstandclimaticchangessomestudiesshowedthatupto42ofspeciesincertaingeographicalareasareatriskofextinc-tioninthelongtermduetodeforestationandhabitatfragmentationsolely(SodhiKohBrookampNg2004)

TheAsianhighlandsthehighmountainousareasofAfghanistanBhutanChinaIndiaMongoliaNepalPakistanandRussiacontainrichbiological diversity andprovide important ecosystem servicesfordownstreamhumancommunitiesThe regionhasalso someofthegreatestspeciesendemismontheplanetandthegreatvariationinclimatetopographyandelevationunderpinsrichculturaldiversity(Xuetal2009)Howeverclimatechangehasgreatlyimpactedbothbiological diversity and ecosystems services in these areas (Aryal

BruntonampRaubenheimer2014KujalaMoilanenAraujoampCabeza2013 Xu et al 2009) The variation of climate effects that havebeendetectedintheAsianHighlandsshowsprogressivesubstantialchangesatseverallevelsfromspeciestoecosystems(YuLuedelingampXu2010)Impactsofclimatechangeonthehydrologybiodiversityandecosystemsinthisareahavebeenreportedwhichincludegla-cialmeltingchangesinstreamflowgroundwaterscarcityaltitudinalshiftsreductioninplantandanimalhabitatsbiodiversitylossandgrasslanddesiccation (PresseyCabezaWattsCowlingampWilson2007ShresthaampBawa2014Waltheretal2002)Furthermoremany studies foresee that future climate changewouldhaveevengreaterimpactsonbiodiversityinCentralAsia(ChenLiDengFangampLi2016GarciaCabezaRahbekampAraujo2014ZhangZhangampSanderson2013)ItisimportanttounderstandtheresultsofthesechangesintermsofhabitatcompositionstructureandfunctionandtheresponsesofanimalgeographicaldistributionwhichcanguideconservationactionsandgovernmenteffortsintheAsianHighlandsinresponsetothesechanges(XuampGrumbine2014)

Brown bear (Ursus arctos) is a solitary non-territorial specieswithapromiscuousorpolygamousmatingsystem(JerinaJonozovicKrofelampSkrbinsek2013Figure1)Ithasacircumglobaldistribu-tion in thenorthernhemisphereoccurring inNorthAmerica (TheUnitedStatesandCanada)EuropeandnorthernandCentralAsia(McLellanetal2008)Manyoftheseregionsareexperiencingrapidclimatechange (ShresthaGautamampBawa2012) InCentralAsiaandtheAsianHighlandsbrownbeardistribution ismostly limitedtohigherelevationareaswheremorepronouncedeffectsofclimatechangehavebeenreported(Aryal2012Aryaletal2014)Intheseregionsbrownbeardistributionandpresencemaybeimpactedbychanging thermal regimes vegetation and prey abundance Suchchangesmaypotentiallyincreasehumanndashbearconflictsduetoshift-ing indistributionof resources andpossibly increasing scarcityofkeyresourcessuchaswaterandfoodInthesamewaydecreaseinspeciesdiversityintheregionduetoclimatechange(BertelsmeierLuqueampCourchamp2013Seimetal2016)mightdirectlyaffectthedistributionandabundanceofthebrownbearbyreducingfoodresources Reduced food abundancemay result in increased inci-dencesofbrownbearsmovingtoanthropogenicareasinsearchoffoodwhichcouldleadtoincreasedlevelsoflivestockdepredationand humanndashbear conflictHowever little is known regarding how

FoundationofChinaGrantAwardNumber31460566and31760706 protectedareasmayforcebrownbearstomoveoutsidetheprotectedareasthereby

increasingtheirriskofmortalityThereforemoreprotectedareasshouldbeestab-lishedinthesuitablebrownbearhabitatsinfuturetosustainpopulationsinthisre-gionFurthermoredevelopmentofcorridorsisneededtoconnecthabitatsbetweenprotectedareasofdifferentcountries inCentralAsiaSuchpracticeswill facilitateclimatemigrationandconnectivityamongpopulationsandmovementbetweenandwithincountries

K E Y W O R D S

AsianhighlandsbrownbearCentralAsiaclimatechangehabitatshiftspeciesdistributionmodel

















3emsp |emspRESULTS






439 583


271 02


52 27


44 22


Elevation 43 73

Aspect 23 17


21 144

Slope 21 08

Landcover 12 1


1 47




05 07












0519 0000


0334 0046












Mongolia 47750300 1387 46588000 minus243





Uzbekistan 1027170 030 1552340 5113

China 225981000 6566 196961000 minus1284

India 14100200 410 10388200 minus2633

Bhutan 1418210 041 1308400 minus774

Nepal 4050590 118 3513230 minus1327

Pakistan 6850260 199 5650130 minus1752

Total 343049390 305163260 minus1104





























Mongolia 6052740 6270320 359





Uzbekistan 527812 640147 2128

China 94067200 92783100 minus137

India 3312480 2416220 minus2706

Bhutan 557279 611163 967

Nepal 1873680 1859730 minus074


Total 112433024 110391256 minus182




ACKNOWLEDG MENTS







ORCID




R E FE R E N C E S















































































































3emsp |emspRESULTS






439 583


271 02


52 27


44 22


Elevation 43 73

Aspect 23 17


21 144

Slope 21 08

Landcover 12 1


1 47




05 07












0519 0000


0334 0046












Mongolia 47750300 1387 46588000 minus243





Uzbekistan 1027170 030 1552340 5113

China 225981000 6566 196961000 minus1284

India 14100200 410 10388200 minus2633

Bhutan 1418210 041 1308400 minus774

Nepal 4050590 118 3513230 minus1327

Pakistan 6850260 199 5650130 minus1752

Total 343049390 305163260 minus1104





























Mongolia 6052740 6270320 359





Uzbekistan 527812 640147 2128

China 94067200 92783100 minus137

India 3312480 2416220 minus2706

Bhutan 557279 611163 967

Nepal 1873680 1859730 minus074


Total 112433024 110391256 minus182




ACKNOWLEDG MENTS







ORCID




R E FE R E N C E S









































































































Mongolia 47750300 1387 46588000 minus243





Uzbekistan 1027170 030 1552340 5113

China 225981000 6566 196961000 minus1284

India 14100200 410 10388200 minus2633

Bhutan 1418210 041 1308400 minus774

Nepal 4050590 118 3513230 minus1327

Pakistan 6850260 199 5650130 minus1752

Total 343049390 305163260 minus1104





























Mongolia 6052740 6270320 359





Uzbekistan 527812 640147 2128

China 94067200 92783100 minus137

India 3312480 2416220 minus2706

Bhutan 557279 611163 967

Nepal 1873680 1859730 minus074


Total 112433024 110391256 minus182




ACKNOWLEDG MENTS







ORCID




R E FE R E N C E S



























































































































Mongolia 6052740 6270320 359





Uzbekistan 527812 640147 2128

China 94067200 92783100 minus137

India 3312480 2416220 minus2706

Bhutan 557279 611163 967

Nepal 1873680 1859730 minus074


Total 112433024 110391256 minus182




ACKNOWLEDG MENTS







ORCID




R E FE R E N C E S


































































































ACKNOWLEDG MENTS







ORCID




R E FE R E N C E S































































































decreasing brown bear (ursus arctos) habitat due to climate...

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