BROWNBEARFOODHABITSATTHEBORDEROF ITSRANGE: ALONG-TERMSTUDY
JAVIER NAVES,ALBERTO FERNA´NDEZ-GIL,CARLOS RODR´IGUEZ,*AND MIGUEL DELIBES
Departamento deBiolog´ıa deOrganismosySistemas,Universidad deOviedo,Catedra´tico
RodrigoUr´ıas/n,Oviedo33071,Spain(JN,AF-G,CR)
DepartmentofAppliedBiology,Estacio´nBiolo´gicadeDon˜anaCSIC,AvenidaMar´ıaLuisas/n, Sevilla41013,Spain(JN,AF-G,CR,MD)
Brownbear(Ursusarctos)foodhabitswereexaminedfrom1,500fecalsamplescollectedbetween1974and
2004intheCantabrianMountainsofnorthernSpain.Themost importantfooditemsweregraminoidsandforbs inthespring,fleshyfruits(especiallybilberries)inthesummer,andhardmastintheautumnandwinter (especiallyacorns).Animalmatteralsowasconsumedthroughouttheyear.Wefounddifferences between3 brownbearpopulationnuclei within theCantabrianpopulation,which could beofenormousinterestforhabitat management.Wealsoinvestigatedhowmuchinterannualvariationindifferentfooditemsinfluencedourdiet estimates.Highfluctuationsamongyearsratherthanvaluesaroundameanwereinherenttosomefooditems. However,for otheritems,themean seemstobeareliabledescriptor.Wefoundthattheadditionalyearsofdata increasedthecoefficientofvariationassociatedwithsomeofourdietestimatesandsuggesttheexistenceof directionalchangesinbrownbearfoodhabitsthathavebeenlargelyneglected.Althoughsomestudiessuggest thatdietisfixedandnotchangeable,ourresultsshowthatlong-termdietstudiesmayrevealchanges inhabitat usepatternsorhabitatcompositionforbrownbearsandotherwildlifespecies.Thus,incorporatingdietstudies intomonitoringprotocolscanbehelpfulfordesigningandevaluatingbothcurrentandfuturemanagement actions.
Keywords: CantabrianMountains, fecalanalysis,interannualvariation,long-termdietstudy,Ursusarctos
Thebrownbearisoneofthefewlarge-bodiedmonogastric animalsthatobtainsmostofitsenergeticrequirementsfrom plantmatter.Thisforcesbearstospendahighproportionof theirdailyactivityinfeeding(LeFranc etal.1987;Stelmock andDean1986).Inaddition, because ofwinterhibernation, bearsmustaccumulatesufficientfatlayerstofuelmetabolic andreproductive costsduringdenning.Thus,foodhabitsare pivotalinbrownbear ecologyandbehavior(GendeandQuinn
2004;Swensonetal.1999;Welchetal.1997).However,few
studieshaveaddressedtheimportanceofdietcompositionfor managementandconservation (butseeClevengeretal.1992; Craighead etal.1995;Hilderbrandetal.1999).
IntheCantabrian MountainsofnorthernSpainlivesa remnantpopulationofbrownbears (Fig. 1).Thispopulationis consideredthreatenedbytheInternational Unionforthe Conservation of Nature and Natural Resources (Servheen etal.1999)andiscategorizedascriticallyendangeredinthe
*Correspondent:
Spanish Red List of Endangered Mammals (Naves and
Ferna´ndez2003).Thedistributionrangeisfragmentedinto
2subpopulationswithanestimatedpopulationsizeof50–65 individualsinthewest,and20–25intheeast(Clevengeretal.
1992;NavesandPalomero1993;Wiegandetal.1998).The easternsubpopulation mainlyoccupiessouth-facingslopesof suboptimalnaturalhabitatandrelativelylowhumanimpact, whereasthewesternsubpopulation occursmainlyonnorth- facingslopeswithhighhumanimpact butotherwise good naturalquality(Navesetal.2003;Wiegandetal.1998).Inthe westernsubpopulation,thereductionofhuman-inducedmor- talityhasbeenidentifiedasthekeystoneforpopulationre- covery(Servheen etal.1999;Wiegandetal.1998),butsome fooditems(beehives, livestock, andorchards)bringbears increasinglyinto conflictswith humans(Clevengeretal.1992; Mattson etal.1991;seealsoHuygensetal.2003).Thus,the documentationoffoodhabitsisessentialforeffectiveman- agement policies.
We studiedbrownbearfood habitsbyanalyzing1,500 fecal samplescollectedintheCantabrian Mountainsofnorthern SpainbetweenSeptember 1974andMay2004.Although Clevenger etal.(1992)discussedthistopic,theymainly focused on the eastern subpopulation, whereas the larger
FIG.1.—Distributionrangeofbrownbearsinthe CantabrianMountainsofnorthernSpain.The3study areasweredelineatedbasedonhabitat featuresandsightingsoffemaleswithcubs(FWC)onagridof2.5x2.5km.ThedottedlineindicatestheLeitariegosMountainPass.
westernsubpopulationremained almostunattended(butsee Bran˜a et al. 1977, 1988; Garzo´n and Palacios 1979). In addition,pastanalysesonlycoveredshorttimeperiods(,5 years).To ourknowledge,thisis the1ststudytoanalyzelong- termfoodhabitsinanyEurasian brownbearpopulation.This long-termstudynotonlyallowsustodetectsporadicuseof rarefooditems(Craigheadetal.1995;Mattsonetal.1991),but alsotoincludesupra-annual schedulesofmastproducersthat involvebothhighandlowannualseedproductions(Herrera etal.1998).
Ourgoalsweretodescribebrownbearfoodhabitsinthe Cantabrian populationonthebasisofalong-termdataseries, toinvestigatewhetherfoodhabitsdifferamongdifferentareas withinthepopulation,toassesstheroleplayedbythehigh trophicplasticityofbrownbearsinourestimates anddiet descriptions,andtoevaluate howadditionalyearsofdietdata influenceestimatesofvariationofsingledietitems.
MATERIALSANDMETHODS
Studyarea.—Ourstudy area includes the entire range of the CantabrianMountainsinthenorthwesternIberianPeninsula(Fig.1). Thesemountains runeast–westalongtheAtlanticcoast,witha maximum elevationof2,648mandaverageelevationsofnorth-and south-facingslopesof700 m and 1,300m,respectively,and gradients of34%and21%.Thechain’sproximity totheoceanandthe geographic orientation resultsinhighrainfall onthenorth-facing slopesandarainshadowonthesouthernslopes(average annual rainfallof900–1,900mmonthenorth-facingslopesand400–700mm onthesouth-facingslopes).Thismountain rangecontainsthelargest portion of the remnant Atlantic deciduous forest on the Iberian
Peninsulaandconstitutesthesouthernmostboundaryofthissystem
(Garc´ıaetal.2005;PoluninandWalters1985).
Woodlandcoverismorevariedonnorth-facing slopes,withoaks (Quercuspetraea,Q.pyrenaica,andQ. rotundifolia),beech(Fagus sylvatica),birch(Betulaalba),andchestnut(Castaneasativa) trees, whereassouth-facingforestsaredominatedbydeciduousdurmastoak (Q.petraeaandQ.pyrenaica) andbeech.Above1,700–2,300m, climatic conditionspreventforestgrowth,andsubalpineshrubs (Juniperuscommunis,Vacciniummyrtillus, V. uliginosum,and Arctostaphylosuva-ursi)dominate.StandsofErica,Citysus,Genista, and Callunavulgarisalso are common at this altitude. Human densitiesare12.1and6.1inhabitants/km2forthewesternandeastern bearsubpopulations,respectively (Reques1993).Wedistinguish between3localstudyareas:central,western,andeastern.Wesub- dividedthewesternsubpopulationintoacentralandawesternarea
becausetheLeitariegosMountainPass(Asturies–Leo´nprovinces)acts asanaturalbarrier(Fig.1).There,roads,skiruns,andaconcentration ofvillageslargelyinhibitbearmovementsbetweenthe2areas.In addition,westoftheconstriction,limestonealmostdisappearsand forestcoverishigherthaneastoftheconstriction(45%compared to35%),asisthepercentageofoak-forestcover(13%comparedto
6%,respectively).
Feces collection andanalyses.—Wecollected1,500fecalsamples between1974and2004,withvaryingintensity. Mostofthe collections(90%)weregatheredin1980–1987and1994–2002.In the1stperiod,fecalsampleswerecollected duringrandomly dis- tributedtrekswithinthebrownbearCantabrian rangethataimedto allocatebothdailybedsanddenningsites.Inthe2ndperiod,fecal samplesweremostlycollectedduringsystematic surveysbythe BrownBearMonitoringProgram.Thisconsistedofapproximately3- h-longtransectsacross2.5-kmuniversaltransversemercator squares wherebearsignswereseasonallyaccountedasanindexofpresenceor
absence ofthespecies inthestudyarea. Fecalsamples sporadically collectedbyotherresearchers andexperiencedrangersalsowere included.Inbothperiodsneitherradiotracked bearsnorplacesof reportedbear activitywereused,sosamplebiasesduetotheseeffects areirrelevant.Fecalsampleswereeitherair-driedorfrozenbeforethey weredissectedoveratrayandalldietitemswereidentified(without meshscreening)tothe finesttaxonomicresolutionpossible.Weavoid meshscreeningbecausesomefoods(mainlyforbsandsomefleshy fruits)areeasilyidentifiableifsoftdissection wasused,butmodified andevendestroyedbymeshscreening.Inaddition,oneofus(JN) hasobserved thatsomesmallfooditemssuchasantstendtobe misquantifiedwithmeshscreening.Fooditemswereidentifiedby usingmammalhairkeys(Dziurdzik1973;Faliuetal.1980;Teerink
1991)andbotanicalcollections offruits,seeds,andhistological sections(Departamento deBiolog´ıadeOrganismosySistemas, UniversityofOviedo,Oviedo,Spain).Afterdissection,thepercentage volumeofeachiteminthescatwasvisuallyestimated.Thisestimation wasstandardizedamongdifferentobserversbytheseniorauthorto minimizepotentialeffects ontheresults.
In our analyses,we reliedon phenologicalperiodsratherthan
oncalendar months.Weassumed thatforaging begins(andalso vegetativegrowth)whenbearsleavetheirwinterdeninearlyspring. Thisperiodischaracterizedbylowfoodintake(hypophagia)and coincideswithestrusandthematingseason(Ferna´ndez-Giletal.,in press;Mattsonetal.1991).Assummerprogresses,ambientconditions becomedrierandfleshyfruitsstarttoripeninlateJune–earlyJuly.The bears’ foodintakeincreases markedly, allowingthemtogainweight untiltheyenteradenforhibernation inNovember–December (CraigheadandMitchell1982;LeFranc1987).Werefertothese3 periodsasmatingseason(April–June), hyperphagicseason(July– November),andwinter(December–March). Wedescribediet compositionbysummarizingthefrequencyofoccurrenceofeach dietitemanditspercentagevolumeforeachareaandseason.
Tosimplifybothdietdescriptionsandanalyses,andtoallowforthe comparisonwithotherbrownbeardietstudies,wetalliedfooditems into4major groupsby19taxa(seeAppendixI).Forageneral description ofbrownbeardietintheCantabrian Range,andfor statisticalanalyseswhere wewereabletocorrectfordifferentsample sizes,we usedthe entiresample.For seasonandarea-specificdescrip- tions, weonlyuseddatayears with 20scatsforthehyperphagic seasonand 8 scats for the simplerdiets of matingand winter seasons.Toobtaintheseminimumsforeachseason,wechosetheyear withthehighestsampleandcalculated thecontributiontothedietof eachofthemajor foodgroupsonthebasisof1scat,2,3,andsoon, choseninrandomorder,andwerepeatedthisprocess9times.We calculatedthecoefficientofvariation(CV)ofthe10runsforeach simulated samplesizeandminimum samplesizesweresetwhenthe CVforallfoodgroupswerebelow1.Thisarea-specificdescription wasnotconducted fortheeasternareabecauseofthemorescattered andopportunisticsamplingschemethere.
Statisticalanalyses.—We used generalized linear models to
investigatethe differencesin brown bear diet betweenour study areas.Weusedthepresence orabsenceofmajor(above3%oftotal volumeineachseason)fooditemsineachscatasresponse (depen- dent)variablesandarea(western,central,oreastern) asexplanatory variable. Becausewefocusedonthepresence orabsenceoffood items,tracesmaypotentiallybeanalyzedequaltoafoodconstituting asubstantialportionofthescat.Toavoidthis,weonlyconsidered fooditemsthatoccurredatavolume.9%.Webuiltgenerallinear modelswithS-Plussoftware(Professional,release2Mathsoft,Inc., Seattle,Washington)usingabinomialfunctionforerrorsandalogit link.Forcomparinglevelswithinafactor,weselectedthecontrast
treatmentoption,wherethe1stlevelisassignedthevalue0(aliased withintercept)andthenotherlevelsmeasure thechange fromthe1st level.Becausetherelativeimportanceofeachfoodvariedamong seasons(P,0.001forallfooditemsexceptforinsects[P¼0.03]and vertebrates[P¼0.01]),separatemodelswerederivedforeachseason. Becauseofthehighnumberoffooditemspresentinthehyper- phagicdietofthecentralarea,weusedprincipalcomponentanalysis (PCA)asadatareductionmethod.PCAwasperformedonthe10most commonfooditems(ahighernumberofitemscaused ill-conditioned results).TheobjectiveofPCA,otherthanreducingthenumberof independentvariables,wastoidentifythoseitemsthattendtooccur
togetherandthosethattendtooccurseparately.
RESULTS
Morethan100taxa(25speciesofberriesandfleshyfruit,
7species ofhardmast,morethan60species ofgreenvegeta- tionmatter,andabout30animalspecies)wereidentifiedas fooditemsforbrownbearsintheCantabrian Range(Table1; AppendixI).Halfofthesampleshowedmonodiets,andin
79%ofthefecal samples,asinglefooditem representedmore than75%ofthetotalvolume.
Dietin thewinterseason.—Rough fieldconditionsand
lowerbearactivitybecauseofwinterdormancy causeda smaller samplesizeforthisseason.Hardmastwasthemost importantfoodsupplyduringwinterforCantabrian bears, togetherwithgraminoids andforbs(Tables1and2).Con- sumptionofalmostallwinterfoodsdiffered betweenareas (Table3);chestnuts wereabsentintheeasternarea,and hazelnuts(Corylusavellana)wereonlypresentinthewest. Graminoidswerethemostimportantandconstantwinter food forbearsinthecentralarea,whereasgraminoidsarealmost absentinthewest(Table2). There,bearsmainlyfedonacorns andbeechnuts,althoughthelattershowedahighinterannual variationinitscontribution towinterdiet.Therelativeim- portanceofbothbeechnutsandapples(Malus) inthecentral areaalsochangedmarkedlyfromyeartoyear(Table2).
Dietofmatingseason.—Inthematingseason,Cantabrian
bearsmainlyfedonforbsandgraminoids,butalsoateanimal matteraswellasacornandbeechnutcropsfromtheprevious autumn(Table1).Occurrence offorbs,beechnuts, andacorns differedbetweenareas(Table4).Area-specificdescriptions (Table2)showedthatforbswerethemostimportantandcon- stantfooditemforbearsbothinthecentralandwesternareas. Graminoidsalsowereconsumedwithlowinterannualfluctua- tionsinthewesternarea,butmoreirregularlyinthecentral area.Amongoverwinteringhardmast,westernbearsfedon acorns,whereascentralbearsfedonbeechnuts.Bothshowed ahighinterannualvariationintheirconsumption.Vertebrates wereconsumedmostfrequentlyduringthisperiod;however, CVvaluesforvertebratessuggesthighinterannualfluctuations. Dietofhyperphagic season.—Berries,fleshy fruits, and hardmastconstitutedthebulkofthediet,althoughbearsalso consumedherbaceousplants(mainlyforbsandgraminoids) andanimalmatter(Table1).Amongfleshyfruits,onlyblack- berries(Rubus), andSorbusfruitswereconsumedinsimilar proportionsinall3areas(Table5).Bilberries(Vaccinium) weremorefrequentlyconsumedinthewesternarea,where
TABLE 1.—SeasonalfrequencyofoccurrenceandmeanpercentagevolumeoffooditemsindietofbrownbearsintheCantabrianMountainsof Spain.nis numberofspeciesortaxa includedineachfoodcategory(seeAppendixI).Asterisks(*)identifyfooditemsincludedintheanalyses. Digestibility (D)isincluded,whereknown,aspercentageofdrymatter(seePritchardandRobbins1990).Samplesizeisthenumberoffecal samplesineachseason.
FooditemsnD Herbs
WinterMatingHyperphagic
FrequencyVolume(%)FrequencyVolume(%)FrequencyVolume(%)
*Forbs / 34 / 45 / 12.2 / 5.2 / 58.7 / 45.4 / 14.1 / 6.7*Graminoids / 18 / 24.4 / 17.3 / 38.8 / 20.3 / 19.8 / 7
Totalherbs / 65 / 37 / 22.4 / 76 / 65.7 / 29.2 / 13.6
Fleshyfruits
Arbutus / 1 / 0.5 / 0.3 / 1.1 / 0.5Arctostaphylos / 1 / 0.1 / 0.0
Crataegus / 1 / 1.9 / 0.8
Frangula / 1 / 0.5 / 0.4 / 1.9 / 1.5
*Malus / 2 / 6.8 / 2.5 / 1.1 / 0.2 / 13.8 / 7.6
*Prunus / 4 / 1.4 / 1.1 / 10.9 / 6.8
*Rhamnus / 1 / 10 / 7.3
Rosa / 1 / 2 / 1.6 / 1 / 0.5
*Rubus / 3 / 1.9 / 0.8 / 7.9 / 3.1
*Sorbus / 2 / 5.6 / 2.7
*Vaccinium / 2 / 65 / 0.5 / 0.2 / 0.6 / 0.1 / 16.4 / 11.3
Other / 6 / 0.8 / 0.1 / 0.5 / 0.2
Totalfleshyfruits / 25 / 9.8 / 5 / 5.8 / 2.3 / 58 / 42.4
Hardmast
*Castanea / 1 / 13.7 / 11.8 / 0.8 / 0.6 / 8.4 / 7*Corylus / 1 / 3.4 / 2.9 / 11.9 / 6.4
*Fagus / 1 / 11.7 / 9.5 / 5.3 / 3.8 / 3 / 2.3
*Quercus / 3 / 49.3 / 42.6 / 16.3 / 13.4 / 21.6 / 16
Totalhardmast / 7 / 72.7 / 66.8 / 22.2 / 17.8 / 41.6 / 31.6
Animal
*Insects / 13 / 4.9 / 1.1 / 18.6 / 4.4 / 16.5 / 4.5
*Vertebrates / 19 / 94 / 10.7 / 3 / 19.4 / 9.3 / 15.2 / 6.9
Totalanimal / 32 / 15.6 / 4.2 / 36 / 13.7 / 29.8 / 11.4
Samplesize / 205 / 361 / 934
Rhamnus fruitswereabsent.Apples(Malus) weremore frequentlyconsumedinthecentralandeasternareas(Table
5).Amonghardmast,acornswereconsumedlessinthecentral areathanintheother 2areas.Chestnutswererarelyconsumed inthewestduringthisperiod.Nodifferencesamongareaswere foundintheconsumption ofanimalmatterduringthe hyperphagicperiod(Table5).
Someofthedocumenteddifferencesamongareasaredue tothesparser easternarea, whereseveral fooditems(cherries [Prunus],hazelnuts,andchestnuts)thatwerecommoninthe otherareaswererare.Bearsalsoconsumedahigherproportion ofgraminoids andforbs(16%and14%oftotalvolume, respectively;n¼98scats).
Area-specificdescription(Table2)showedthatthedietof thewesternareawascharacterizedby3predominantfooditems thatripensequentially: cherriesarereplacedbyVaccinium fruitsatmid-summer,whicharesubstitutedbyacornsatthe endofthisseason.These3itemscomprisedmorethanhalf ofthedietduringthehyperphagic seasoninthewesternarea andshowedarelatively lowinterannualvariation.Theywere complementedwithherbs,animalmatter,andotherhardmast andfleshyfruits,butallinvolumeproportions,10%.
Ascomparedtotheother2areas,thecentralareashowedthe mostdiverse,complex,andfluctuatingdiet.Infact,nosingle item(neitherhardmastnorsoftmast[berriesandfleshyfruits]) comprised.13% oftotalvolumeinthehyperphagicperiod, andthemajorityofitemsshowedhighvaluesofCV(Table2). WhenPCAwasperformedonthe10mostcommonfooditems, theyweregroupedin3componentsthataccountedfor34%,
21%,and15%ofthevariance,respectively(Fig.2).Principal component1groupedfoodsfromlowlands (mainlyapples, chestnuts,andcherries)atnegativeloadings,andfoodsfrom uplands(graminoids, Vaccinium,andRhamnus)atpositive loadings.Principalcomponent 2describedgroupsinaccor- dancewiththeuseofforestedareas.Hardmastfromforests (acornsandhazelnuts) appearedatnegativeloadings;verte- brates, Vaccinium,andRhamnusfruitsappeared atpositive loadings,andtheymainlyoccur(atleastthelast2)inopen shrublands.Principal component3describedtheimportant contributionofherbstobrownbeardiet, becausebothgramin- oidsandforbs(negative loadings)werethemainvariables affectingthis3rdcomponent(Fig.2).
Profiting fromourlong-termdataseries,wecalculatedthe accumulatedvalueoftheCVforeachfooditembyincluding
TABLE 2.—Seasonal meanpercentagevolumeandcoefficientofvariation(CV)offooditemsindietofbrownbearsin2ofthestudyareas (CantabrianMountainsofSpain).Differencesamongyearsintherelativecontributionofanyitemtodiet(testedbyrunninggenerallinearmodels wherethefactoryearwasconsideredasexplanatoryvariable)arenotedby anasterisk(*).Formoreclarity,contributionsbelow3%areindicated byt(¼trace).Sampleindicatesthenumberoffecalsamplesfollowed(inparentheses)bythenumberofdata-years.
WinterMatingHyperphagia
CentralWesternCentralWesternCentralWestern
Item
XCVX
CVX
CVX
CVX
CVXCV
Graminoids / 40.17 / 0.7* / 22.5 / 1.3* / 20.04 / 0.55 / 10.03 / 0.8* / 3.22 / 0.19Forbs / 9.25 / 0.97 / 53.16 / 0.5* / 55.61 / 0.6* / 6.47 / 0.8* / 4.46 / 0.65
Rhamnus / 12.83 / 0.9* / t
Sorbus / t / t
Rubus / 3.27 / 1.2* / 3.34 / 1.26
Prunus / 3.19 / 1.38 / 6.23 / 1* / 10.18 / 0.9*
Malus / 10.06 / 2.1* / t / t / 6.86 / 1.3*
Vaccinium / t / t / t / 9.73 / 1.5* / 23.21 / 0.6*
Castanea / 11.11 / 1.7* / 17.61 / 1.4* / t / t / 4.68 / 1.7*
Quercus / 12.20 / 1.5* / 38.27 / 1* / t / 7.47 / 1.66 / 11.11 / 1.6* / 25.00 / 0.9*
Fagus / 7.92 / 2.1* / 33.44 / 1.7* / 5.52 / 1.6* / 3.49 / 2.9*
Corylus / 4.37 / 1.7* / 7.18 / 1.5* / 6.88 / 0.34
Vertebrates / t / t / 10.63 / 1.3* / 11.50 / 1.5* / 8.78 / 0.54 / 6.73 / 0.58
Insects / t / 3.14 / 1.25 / 3.83 / 0.80 / 8.00 / 1.4*
Sample / 62(5) / 76(3) / 165(7) / 92(5) / 531(10) / 191(5)
data-years inastepwisefashion.Forapples,cherries,insects, andchestnuts,theCVdecreasedwithadditionalyearsofdata (Fig.3).However,thiswasnotageneralpatternandformany fooditems(forbs,graminoids,Quercus,andvertebrates),the CVremained the same regardless of the number of data years used. For several food items (hazelnuts, Vaccinium andRhamnus fruits,andbeechnuts)theCVincreasedwhen additionaldatayearswereadded(Fig.3).
DISCUSSION
BrownbearsintheCantabrian Mountains,asintherestof Europe,showedomnivorousfoodhabitswithahighproportion ofplantmatterintheirdiet.Ourresultshighlighttheimpor- tanceofbothacornsandbilberries(Vaccinium) asessential fooditemsforbrownbears.Thus,oakforestsandheathlike formations ofclumpedshrubsofVacciniumshouldreceive high conservationprioritiesas criticalforaginghabitatsfor thisendangered species.Managers shouldrestrictdomestic ungulates(whichfeedon boththeplantand theirfruits— Ferna´ndez-Calvo and Obeso 2004) from accessing these
Vacciniumformations.Additionally,mountaintourism,which negativelyimpactsbears(Navesetal.2001;Whiteetal.1999), shouldberestrictedduringlatesummerandearlyautumnwhen bearsareusingtheseareas heavily. Wealsosuggestagreater efforttolimithunting(especiallyduringautumnandwinter) andtoavoidsubcanopyclearingsinold-growthoakforests. Theopeningofnewtracksacrosstheforest shouldbealso avoidedbecausetheydiminish theamountofsuitablehabitat forbearswhileincreasingfragmentation.
ThejointoccurrenceofacornsandfruitsofVacciniuminthe
brownbeardietisrarelydocumented.Thosepopulationsfeed- ingonmastitemsfromdeciduousforests (mainlyEurasian populationsbelow508Nlatitude, andextinctNorthAmerican populations—Brown1985inJacobyetal.1999)seldomcon- sumedfruitsfromVaccinium(Berducouetal.1983;Cicnjac etal.1987;Fabbri1987;FrackowiakandGula1992;Mertzanis
1992;OhdachiandAoi1987;VaisfeldandChestin1993).On thecontrary,thenotableproportionofmoremeridional(i.e., Mediterranean)fooditems(e.g.,Arbutusunedo,C.sativa,and Q.rotundifolia)foundintheCantabrianbear’sdietissimilar to those found in other southern European populations,
TABLE 3.—Modelsthatconsideredareaasanexplanatoryvariableforoccurrenceofmajorfooditemsduringwinter indietofbrownbears in theCantabrianMountainsofSpain.Contributiontodietofeachitemisshownasfrequencyofoccurrenceandpercentageoftotalvolumeinthe period.Valuesshownareparameterestimates6SEandpercentagesofexplaineddeviance(onlyprovidedforsignificantmodels).
ItemFrequency(%)VolumeInterceptCentralareaWestern areaEasternareav2P
Deviance explained (%)
Quercus / 49 / 43 / —0.960.2 / 0 / 1.360.3 / 1.360.4 / 19.56 / ,0.0001 / 7Graminoids / 24 / 17 / —0.360.2 / 0 / —2.260.5 / —1.960.6 / 34.63 / ,0.0001 / 16
Castanea / 14 / 12 / —2.760.5 / 0 / 1.360.5 / 0.160.9 / 8.75 / 0.01 / 6
Fagus / 12 / 10 / 2.19 / 0.33
Forbs / 12 / 5 / —1.660.3 / 0 / —2.360.8 / —0.660.7 / 13.47 / 0.001 / 11
Vertebrates / 11 / 3 / 2.1 / 0.35
Corylus / 3 / 3 / Absent / Present / Absent
TABLE4.—Modelsthatconsideredareaasanexplanatoryvariableforoccurrenceofmajorfooditemsduringthematingperiodindietofbrown bearsintheCantabrianMountainsofSpain.Thecontributiontodietofeachitemisshownasfrequencyofoccurrenceandpercentageoftotal volumeintheperiod.Valuesshown areparameterestimates6SEandpercentagesofexplaineddeviance(onlyprovidedforsignificantmodels).
Deviance
Item / Frequency(%) / Volume / Intercept / Centralarea / Westernarea / Easternareav2Pexplained (%)Forbs / 59 / 45 / 0.660.2 / 0 / —0.160.2 / —2.860.5 / 60.81 / ,0.001 / 12
Graminoids / 39 / 20 / 3.0 / 0.22
Vertebrates / 19 / 9 / 0.79 / 0.67
Insects / 19 / 4 / 3.1 / 0.21
Quercus / 16 / 13 / —3.460.4 / 0 / 1.060.5 / 4.260.5 / 115.2 / ,0.001 / 37
Fagus / 5 / 4 / —2.460.3 / 0 / —1.760.8 / —7.861.3 / 12.9 / 0.002 / 9
includingAbruzzos(Italy),formerYugoslavia,and Greece (Cicnjacet al. 1987; Fabbri1987; Mertzanis1992). Inter- estingly,theCantabrianpopulationistheonlyknowngroupto feedonbothMediterraneanandboreal(e.g.,Vaccinium)foods. Insummary,atthesouthwesternborderofthebrown bear’s Eurasianrange,itsfoodhabitsarecharacterizedbyahigh diversityof fooditems(withasubstantialcontributionoffruits of Rosaceae)that included Mediterranean(e.g., chestnuts), temperate(e.g.,Quercus petraea), andrelict-borealspecies. Whetherthis high trophicdiversityis the resultof a low foragingefficiency(Pykeet al. 1984)oran optimizedresponse todifferentavailabilityofmultiplefooditemsconstitutesan
interestingquestionforfurtherstudy.
Althoughthesefindings areapplicabletotheentireCanta- brianRange,eachofthestudyareasshowedsignificantdif- ferences.Acornsconstitutedthebulkofthewinterdietforthe Cantabrian brownbearpopulation.However, bearsinthe centralareaalsoconsumedahighproportionoflow-energy itemssuchasgraminoids (althoughtheirapparentpredomi- nanceiscausedbythelowdigestibilityofthesefoods—see HewittandRobbins1996;PritchardandRobbins1990).Even takingthisintoaccount,thecontribution ofgraminoids tothe dietishighinthisarea.Thisobservation wassurprising becauseacornsprovide muchmoreenergythangraminoids (Craigheadetal.1995;GrodzinskiandSawicka-Kapusta 1970)
andforagingcostofacornsisprobably lower.Apossible explanation isaloweravailabilityofacornsbecauseofcom- petitionwithotherconsumers,reflectedinthehighherbivore densityinthecentralarea(ObesoandBan˜uelos2003).Free- ranginglivestock,andwildungulates,especiallywildboar(Sus scrofa)couldcauseafastdepletionofacornsduringautumn andearlywinter,forcingbearstofeedongraminoidswhen acornsbecomescarce.
Beechnuts(Fagus)also constituteanimportantfoodsupply, especiallybecause beechforestcoverishigherthanoakforest cover(ratioapproximately3:1—Garc´ıaetal.2005).However, beechoftenfailstoproduce fruit, withperiodsofupto4 consecutiveyearsofmastfailure(Clevengeretal.1992).This couldexplainthelowcontributionofthisitemtothetotaldiet andalso whywewerenotabletofinddifferencesamongareas forthewinterseason.
Duringthematingseason, bearsmostly fedonherbaceous plants,butalsoonoverwinteringacorns(Quercus). Infact, acornsconstituted ahighproportionofthedietoftheeastern subpopulation(63%ofvolume;n¼ 57scats).Thiscouldbe explainedbythedeepersnowcovercharacteristicofseveral partsofthisarea.Thispreventsmasteaters—not onlybears, butalsowild boars, reddeer(Cervuselaphus),free-ranging livestock,squirrels(Sciurus vulgaris), rodents(Rodentia), corvids (Corvidae: Corvus),and common wood-pigeons
TABLE 5.—Modelsthat consideredareaasanexplanatoryvariableforoccurrenceofmajorfooditemsduringthe hyperphagicperiodindiet of brownbearsintheCantabrianMountainsofSpain.Thecontributiontodietofeachitemisshownasfrequencyofoccurrenceandpercentageof totalvolumeintheperiod.Valuesshownareparameterestimates6SEandpercentageofexplaineddeviance(onlyprovidedforsignificant models).
ItemFrequency(%)VolumeInterceptCentralareaWesternareaEasternareav2P
Deviance explained (%)
Quercus / 22 / 16 / —1.860.1 / 0 / 0.960.2 / 1.260.2 / 36.25 / ,0.0001 / 4Graminoids / 20 / 7 / —1.960.1 / 0 / —0.360.2 / 0.760.3 / 10.95 / 0.004 / 1.5
Vaccinium / 16 / 11 / —2.460.1 / 0 / 1.660.2 / —0.260.4 / 66.19 / ,0.0001 / 9
Insects / 16 / 4 / 1.39 / 0.50
Vertebrates / 15 / 7 / 2.65 / 0.27
Malus / 14 / 7 / —1.960.1 / 0 / —1.560.4 / 0.360.3 / 27.87 / ,0.0001 / 5
Forbs / 14 / 7 / —2.260.1 / 0 / —0.160.3 / 1.060.3 / 12.38 / 0.002 / 2
Corylus / 12 / 6 / —2.460.1 / 0 / 0.560.2 / —2.260.9 / 16.47 / 0.0003 / 3
Prunus / 11 / 7 / —2.460.1 / 0 / 0.560.2 / —6.866.1 / 24.76 / ,0.0001 / 4
Rhamnus / 10 / 7 / —1.960.1 / 0 / —3.660.9 / —0.260.4 / 47.69 / ,0.0001 / 8
Castanea / 8 / 7 / —2.060.1 / 0 / —1.960.5 / —7.266 / 45.17 / ,0.0001 / 9
Rubus / 8 / 3 / 0.22 / 0.89
Sorbus / 6 / 3 / 3.2 / 0.2
FIG. 2.—Relationships betweenfactorsinprincipalcomponent analysisofdietofbrownbearsinthecentral area(Cantabrian MountainsofSpain).A)Factor1relativetofactor2.B)Factor1 relativetofactor3.Factor1groupedfoodsfromuplands(Vaccinium, Rhamnus,andgraminoids) atnegativeloadingsandfoodsfrom lowlands(Prunus,Malus,andCastanea)atpositiveloadings.Factor2 groupedfoodsfromforestedareas(CorylusandQuercus)atnegative loadings andfoodsfromopenareas (VacciniumandRhamnus)at positiveloadings.Factor3accountedfortheimportantcontribution ofgraminoidsandforbs(asnegativeloadings)tobrownbeardiet.
(Columbapalumbus)—fromaccessing acornsduringwinter. Whensnowmeltsinspring,acornsbecomeavailableforbrown bearsintheeastern area. However, inthewestern andcentral areas,wintercovermayhavebeensufficientlylesstoallow othermasteaters(whichareespeciallyabundantinthecentral area, seeabove)accesstotheacornsduringwinter(see ShimanoandMasuzawa[1995]forsimilar effectsofsnow coveronseedpreservation).
Dietduringthehyperphagicseasonwasthemostcomplex
anddiverse,andhasmajorimplications onbearecologyand behavior(Craigheadetal.1995;LeFrancetal.1987).Asmany as13fooditemscontributedtohyperphagicdietofbearsinthe centralarea,buttheirrelativeimportancechangedfromyear toyear.PCAindicatedthattheseinterannualdifferencesmay
FIG.3.—Cumulativevalueofcoefficientofvariation(CV)foreach fooditem indietofbrownbearsovera10-yearperiod forthecentral studyarea(CantabrianMountainsofSpain)duringthehyperphagic season(shownin2graphstodisplayresultsfor10planttypesand
2animalgroupswithoutcrowding). Somefoodswerenotconsumed atthebeginning,buttheywereincorporated intothegraphupon appearance.
beduetodifferenthabitatselection,whichisprobablydriven byfood availability.Bearscanmostlyfeedoncherries,apples, andchestnutsinlowlands,buttheyalsocanfeedonVaccinium aswellasRhamnusfruitsinuplands.Atmiddlealtitudes,bears wereableto obtaina 3rdfeedingoption(acornsandhazelnuts) fromforests (Fig.3).
Clevengeretal.(1992)documentedthatthebrownbear’s dietintheeasternsubpopulationwaslessdiversethaninother partsoftheCantabrian Range.Despitetheimportance ofdiet composition duringthehyperphagicseasonwhenbearsare storingfatbeforedenning,bearsinthissubpopulationconsume ahighproportionoflow-energyitemssuchasgraminoidsand forbs.Thisprobablyconstrains theamountoffatbearscan accumulateandthuslimitsthetimetheycanspenddenningand thenumberofcubsfemalescanproduceandrear(seeBunnell andTait 1981;Rogers 1987).Thisabundanceoflow-quality fooditemsinthebear’s dietsupportspreviousworkthat characterizedthisareabyitslowernaturalsuitabilityforthe brownbear(Navesetal.2003).Otherauthors alsohave suggestedthepotentialinfluenceoffeedingconditionsduring thehyperphagic periodindenning,documenting ahigher numberofnonhibernating bearsduringyearsoflowfood availability(VaisfeldandChestin1993).Conversely,thereis aconstantpresenceof high-qualityfooditemsinthedietofthe
westernareaalmostannually, supportingthehighernatural qualityofthehabitat,whichalsowasstressed byNavesetal. (2003).
Thedifferences indietcompositionamongthestudyareas
(Tables2–5)highlightedtheimportanceofconsideringlocal scales(brownbearpopulation nuclei)whenstudyingdietsat widegeographicalranges.Inadditiontotheirimplicationsfor dietdescription(seeTables1and2),thesedifferenceshave enormousinterestforbrownbearmanagement, becauseeachof thestudiedareasbelongstoadifferent protectedarea(within theregionalandnationalreservenetwork).Managers ofeach areaarethenresponsibleforproposing,designing,andimple- mentingtheirownmanagement actions.Forinstance,our resultssuggestthatimproving feedingconditions forbears shouldconstituteapriorityformanagersofthecentraland easternareas,whereassuchmanagement seemsnottobe necessaryinthewesternarea.
Manydietstudieshaveassumed(explicitlyorimplicitly)
thatdietisanunchangingcomponentofanimalecology.In fact,someeffortsexisttocalculate thenumberofyearsnec- essarytodetermineinterannualfluctuations inthediet. However,thisonlymakessenseiftheannualcontributions ofafooditemfluctuatearoundamean,andthusthemore data-yearsavailable,themorerobusttheestimate becomes (lowCV). However,long-termstudieshavesuggestedthat environmentalfluctuationsandland-usechangescouldresult inlong-termoscillationsindietcomposition(Mattsonetal.
1991).Examinationofourdatasetsuggestslong-termtrendsin
theavailabilityoruseofsomedietitems,particularlyforfleshy fruits andhardmast,except thoseitemsinvolvedinsupra- annualschedulesofhighlyfluctuatingseedproduction(mainly acornsandbeechnuts—Herrera etal.1998),whichwould requireadditionalstudy.Becauseconclusions drawnfrom manystudiesofbrownbearfoodhabitsareoftenrelevant for management(seeCraigheadetal.1995),theresultsofthis studyindicatethatassessinglocaldifferencesinfoodhabits couldbeofenormousinterestwhenpopulations arespatially structured,andeachofthesubpopulations(ornuclei)could be managedfollowingdifferentcriteria,mainlybecauseoftheir peculiarities,butalsobecauseofadministrativereasons;and thatitisnecessarytoincorporatedietstudiesinmonitoring protocolsforsomeendangered populations.Dietstudiescon- stituteavaluabletooltodetectchangesinhabitatatascalethat maynotbeapparentsolelywithhabitatmonitoring.Directional changesinfoodhabitsduringacertain timeperiodmay provideimportantcuestodesignandimplement management actions,toevaluateactionsalreadyinprogress,orboth.Our resultssuggestthatthesechanges areoccurring intheCanta- brian Range,probablyasthebrownbearsrespondtochanging foodavailabilityorasaconsequenceofchangesinforaging habitat selection (perhaps due to anthropogenic factors). Itremainsachallengetoinvestigate whichenvironmental changeshaveoccurredduringthelastdecadesinthisrangethat couldexplainthesechanges indiet,aswellastoassesstheir potentialeffectsonthebrownbearpopulationfromboththe nutritionalandtheconservationpointofview.
RESUMEN
Seestudianlosha´bitosalimenticiosdelosopardocanta´brico apartirde1,500excrementosrecogidosentreseptiembrede
1974ymayode2004.Lososospardosconsumieronunagran proporcio´ndegram´ıneasymegaforbiasdurantelaprimavera, frutoscarnososduranteelveranoyfrutossecosduranteel oton˜oeinvierno.Dehechoencontramosunagrandiversidad de frutos de especies mediterra´neas, templadas y boreales relictas.Tambie´nconsumieronmateriaanimaldurantetodoel an˜o,aunqueconmenorfrecuenciaenlaestacio´ninvernal.En te´rminos de composicio´n de la dieta, nuestros resultados subrayanlaimportanciadelasbellotasylosara´ndanoscomo alimentosfundamentalesparaelosopardo.Tambie´nencon- tramosdiferenciassignificativasentrelas3a´reasdeestudio, quepuedenserdeenormeintere´spara lagestio´ndelha´bitaten cadaunadeellas. Poru´ltimo,investigamoselpapelquejuega lavariacio´ninteranualcaracter´ısticadeladietadelosopardo ennuestrasestimasacercadelacontribucio´nrelativadelos diferentesalimentos,yportantoenladescripcio´ndeladieta. Usandoelcoeficientedevariacio´n(CV) comomedidade dispersio´nencontramosquealgunosalimentoscontribuyende formama´somenosconstante aladieta,mientrasqueotroslo hacendeformasustancial,peroespora´dica,loquehacema´sdif´ıcilcaracterizarsuimportancia.Tambie´ncomprobamosque alaumentarelnu´merodean˜osconsiderados paracaracterizarla dieta,elCVasociadoaalgunosalimentosaumento´,loque apuntaalaexistenciadetendenciastemporalesensuconsumo quedebera´nserconsideradaporestudiosposterioresae´ste. Asimismo,dichastendenciassugierenlaincorporacio´n de estudiosdedietaalosprogramasdeseguimiento deespecies amenazadas,yaquelejosdeserinmutable,ladietapuedesufrir cambiossustancialesquesirvancomoindicadoresqueayuden a mejorar las medidas de gestio´n disen˜adas para dichas especies.
ACKNOWLEDGMENTS
Manypeoplecontributed tocollectionandanalysesoffeces, especiallyJ.SeijasandA.Ruano.I.C.Ferna´ndez-Calvo,J.Iglesias, M.Rico,andrangersfromthewholeCantabrian Rangewhoalso collectedasignificativenumberofsamples,especiallyJ.M.Carral andA.Ramosinthewesternarea,andA.Gonza´lez,C.Granda,andS. Sen˜asinthecentralarea.WeareindebtedtoP.Jordano,whoprovided usinformationaboutfruitcharacteristics (bymeansofthefruit databaseFRUBASE) andmanyhelpfulcommentsaboutplant ecology.C.Aedo,J.A.Ferna´ndez-Prieto,J.R.Obeso,andT.E. D´ıazhelpedusinidentifying plantremainsinfeces.A.Kraljevic helpedwithcorrectionsoftheEnglishtext.Thispaperisacontribution totheprojectsBOS2001-2391-CO2-02(PlanNacionaldeIþDþI; MinisteriodeEducacio´nyCiencia,Spain),andFremdFþE0302
UFZ-CSIC(Germany-Spain)andweacknowledge J.R.Obeso,andT. Wiegandasresponsibleresearchersoftheseprojects.
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Submitted23September2005.Accepted1March2006. AssociateEditorwasGerardoCeballos.
APPENDIX I
Resultsofscatanalysesatthehighesttaxonomic resolutionfor brownbearsintheCantabrianMountains ofSpain.Aftereachfood item, weshowitsabsolutefrequencyofoccurrence.Forsummarizing categories,thisfrequencyaccountsforbothidentifiedandunidenti- fiedtaxa. Brown bearalso appearedas a food itembecausewe foundsubstantialcontribution ofbear’shairtoscatcomposition, althoughwecannotascertaintheoriginofsuchhairs(i.e.,whetherthey correspondtorealconsumptionornot).Asterisksindicate fooditems determinedatthe specieslevelfromfieldobservationswhencollected (Quercus),or basedonthepresenceof characteristicleavesin the scat (V.uliginosum);however, theseweremadesporadically,andthusall acornswereconsideredasQuercusspecies,andallbilberrieswere conferredtobeV.myrtillus(themainspecies inthestudyarea).
Domestic ungulates (85).—Equus caballus,9; Bostaurus,26;
Caprahircus,13;Ovisaries,1;Susdomesticus, 1.
Wildartiodactyls(61).—Capreoluscapreolus,45;Cervuselaphus,
2;Rupicaprapyrenaica,5;Susscrofa, 1.
Smallmammals(14).—Rodentia, 4;Apodemus,1;Arvicolinae,2;