Abnormal Behaviours in Two Captive Brown Bear (Ursus arctos Linnaeus, 1758) Females: Individual Differences and Seasonal Variations [Abnormales Verhalten in zwei gefangen Grizzlybär-Weibchen (Ursus arctos Linnaeus, 1758): einzelne Unterschiede und saisona

Abnormal

Behaviours

in

Two

Captive

Brown

Bear

(Ursus

arctos

Linnaeus,

1758)

Females:

Individual

Differences

and

Seasonal

Variations

Abnormales

Verhalten

in

zwei

gefangen

Grizzlybär-Weibchen

(Ursus

arctos

Linnaeus,

1758):

einzelne

Unterschiede

und

saisonale

Variationen

Ana

I.

Soriano

,

Dolors

Vinyoles

,

Carmen

Maté

Received6September2016

Abstract

Abnormalbehavioursarecommonincaptiveenvironmentsthatnotsupplythephysicaland psycho-logicalneedsofanimals.Thereareanimals,likebrownbears,moresusceptibletodevelopabnormal behavioursduetotheirseasonalbiologyrelatedtofood,hibernationorreproduction.Thetwobrown bearUrsusarctosfemalesfromBarcelonaZoo,Spain,showedtwodifferentpatternsofabnormal behaviours.Theold♀displayedepisodesofbitingatreetrunkwhiletheyoung♀carriedout head-tossingevents.ThestudiedperiodwasfromMarchtoDecember2004dividedintoseasonalperiods: autumn,springandsummer.Atotalof63hoursofobservationswererecordedusingamulti-focal continuousmethod.Thetimeinvestedonabnormalbehaviourwashigherinspringfollowedby sum-merandautumninbothfemales.Theothervariablesrelatedtotheabnormalbehaviourstudiedwere duration,intensity,occurrenceandspaceusewhichalsoshowedstatisticallysignificantdifferences amongseasonalperiods.Theold_♀spaceuseduringabnormalbehaviourwasinthesamezone mean-whiletheyoung♀showedstatisticallysignificantdifferencesamongseasonalvariationsandzones oftheenclosure.Theseresultsshouldbetakenintoaccounttoimprovethemanagementofbearsin zoologicalinstitutions.

Keywords: Episodes;Events;Stereotypies;Zoomanagement;Spaceuse

∗_{Correspondingauthor.}

Introduction

In orderto achieve good animal welfare inzoological institutions it is necessary to understandthephysicalandpsychologicalneedsoftheanimals andprovideappropriate management.Studiescarriedoutinthenaturalhabitatofspeciesprovidegoodindicators forthespecies-specificrequirementsthatshouldbesuppliedinzoologicalinstitutions.In manycases,the wild–captivecomparisonisausefultoolasananimal-welfareindicator

(Broom,1983;Veasey,Waran,&Young,1996).

Abnormalbehavioursarenotobservedinthetypicalbehaviourpatternsofwildor free-roaminganimals(Criswell&Galbreath,2005;Meyer-Holzapfel,1968)andtheoccurrence ofsuchbehaviourisconsideredanindicatorofpooranimalwelfareinzoological institu-tions.Broom(1983)suggestedthatitisunacceptableforanyanimaltospendmorethan 10%ofthewakingdaydisplayingabnormalbehaviours.Therearedifferentcategoriesof theabnormalbehaviours,includingabnormalescapereactions,refusaloffood,excessive aggression,stereotypicmotorreactions(i.e.head-toss,pacingor straight-line, figure-of-eight,circularandovalcircuits),self-mutilation,abnormalsexualbehaviour(i.e.substitute sexualobjects),apathy,aggression,oralstereotypes(i.e.biting,coprophagy,regurgitation andreingestion,orlicking),abnormalmother–infantrelationshipsandprolongedinfantile behaviour(Fox,1968).Itisnecessarytoidentifyandclassifyabnormalbehaviourscorrectly because,inmanysituations,somebehaviouralexpressionscanbetheresultofphysical dis-ease(e.g.dentalproblems,arthritisorhormonaldysfunctions).Physicalafflictionscanbe detectedthroughveterinarydiagnosesandaredifferentfromthementalconditions associ-atedwithabnormalbehaviour,whichimplicateacomplexneurobiologicalbasis(Mason&

Latham,2004).Onekindofabnormalbehaviourisstereotypicbehaviour,whichis

some-times observedinzoologicalinstitutions andcharacterizedbymorphologicallyidentical movementsrepeatedregularlywithoutanyapparentfunction(Lawrence&Rushen,1993;

Mason,1991;Mason&Rushen,2006).

Members of theUrsidae familyaremorelikelytoexhibitabnormal behaviours,such aspacingorbegging,inzoologicalinstitutionsbecausetheircomplexneeds,particularly relatedtoseasonalvariationsinactivity(hibernation),feeding(omnivorous)or reproduc-tion (polygamous),crepuscular habits andthe extensive territories in nature (territorial behaviour),aredifficulttoprovideartificially(Vickery&Mason,2003a;Ward&Kynaston,

2003).

Individual variationsin abnormal behaviours have also been observed in the Ursids literature.SixtysixbrownbearsUrsusarctosfrom28zoologicalparksshowedindividual patterns(Montaudouin&LePape,2005),andalsoseeninotherspecies;forexample,Giant pandas Ailuropodamelanoleuca(Lindburg,Swaisgood,Zhang,Narushima,&Xiaoping, 2003), Malayan sun bearsHelarctos malayanus(Cheng, 2003),Asiatic black bearsU. thibetanusandMalayansunbears(Vickery&Mason,2003b),andPolarbearsU.maritimus

(Wechsler, 1991). Moreover,individual patterns inabnormal behaviours can be caused

mainlybysevenfactors:gender,hormonallevels,age,nervous-systemmalfunction,time spentincaptivity,typeofrearingorlifeexperience(seeTable1).

Therearefewstudiesthathavestudiedtheeffectsofseasonvariationonbearabnormal behaviours.So,therearetwopublicationsinPolarbearswhereabnormalbehaviourswere

Table1. SeveninfluentialfactorsinthedevelopmentofabnormalbehavioursincaptiveUrsids.

Factor Definition Reference

Gender Inzoologicalinstitutions,malePolarbears showedmoreabnormalbehavioursduringthe springmatingseasonthanfemales

Ames(1993)

Hormonelevels Thereismoretestosteroneinmalebearsduring thebreedingperiod,whichcancauseahigher prevalenceoftheabnormalbehaviours

Lawrenceand Rushen(1993)

Age Theeffectofcaptivityseemstobemore profoundforayoungbearthanformature animals,intermsoftheexpressionand persistenceofabnormalbehaviours

Ridleyand Baker(1982)

Nervous-system malfunction

Usuallyprovokestheappearanceofan abnormalbehaviour

Ridleyand Baker(1982) Timespentin

captivity

Timehasaninfluenceonabnormalbehaviours, whichcanchangeinformwithage;these behaviourscanalsoloseelementsofthe originalbehaviourpatternandevolvewithtime

Lawrenceand Rushen(1993)

Typeofrearing Hand-rearedanimalsseemtohaveagreater tendencytodevelopabnormalbehavioursthan bearsthathavebeenmotherreared

Marrinerand Drickamer (2005) Lifeexperience Thevarietyofexperiencesthatoccurduringthe

lifetimeofeveryanimal(e.g.isolationorpoor environment)canprovokethemanifestationof abnormalbehaviours

Fernandez (2010)

moreprevalentinspringthaninsummer(Ames,1993;Kolter&Zander,1995).Another publication inAmerican black bears U.americanus determined aseasonal variationin abnormalbehavioursandhisrelationshipwithtwospeciestypicalbehaviourswhichwere mate-seekingbehaviour predominatelyinthe latespring andforagingbehaviourinlate summerandautumn(Carlstead&Seidensticker,1991).Thereisnotanypublicationthat describestherelationshipbetweenabnormalbehaviour seasonalvariationandthe space use.

It is crucialtodetermine the importance of the development andpotentiation of the seasonalvariationsincaptivebrownbearsinordertoimproveanimalwelfareandavoid the development of abnormal behaviours. If there are seasonal variationsin abnormal behaviours possibly theremight be also seasonalvariations inother kindof behaviour (e.g.breeding,feedingorrearing).

Theaimofthisstudywasdescribingdifferentaspectsoftheabnormalbehaviours devel-opedby twobrownbearfemales atBarcelonaZoo: individualdifferencesandseasonal variationsoftheduration,intensity,occurrenceandspaceuse.Thiskindofinformation canbeusefulinordertoimprovecaptivebearmanagementbecausetheseanimalsaremore susceptibletodevelopabnormalbehaviours.Thesebehavioursareoneofthemainconcerns forprofessionalsimplicatedincaptiveanimalwelfare.

Materials

and

Methods

The twobrownbearfemales studied atBarcelonaZooarrivedfromthe Parquede la Naturalezade Cabárceno(Cantabria,Spain) inNovember2003.Theyoung ♀ wasborn inCabárcenoon1March1994andrearedbyhermother.Theolderfemale’sbirthtype, location, dateof birth andtype of rearing wereunknown because she wasborn before Cabárcenowasopenedin1990.Thehybridstatusofbothfemalesisalsounknown.

AtCabárcenothesetwofemaleswerehousedtogetherwith80otherbrownbearsina semi-freeroamingreserveforanimals.Theenclosurewasanaturalizedmountainousspace belongingtoanold ironmineandhadatotalareaof63ha.Thediet consistedof fruit, vegetablesandmeatprovidedonceadaywhenavehicleenteredtheenclosure.Thespace didnothaveanyindoorareasandnoenrichmentprogrammewasprovided.

DuringthisstudyatBarcelonaZoo,thetwobearswerehousedtogetherinamoat-style, semi-naturalizedenclosurewithastructureoriginallymadefromcementandatotalarea of 230m2(seeFig.1).Awalldividedtheenclosurewithanopeningtoconnectthetwo parts,eachofwhichhadanaquaticzonefortheanimalstodrinkandbathe.Thefeatures ineachenclosureincludedlivetrees,bushes,severallargestones,largeoverturnedlogsfor climbing,andseveralterracesatdifferentlevelswithanaturalsubstrateofgravel,sandand

Fig.1.Diagramoftheenclosureforbrownbears.AU,honeydispenser;BS,barksubstrate;CAS, waterfall;COS,concretesubstrate;CRS,crushedstonesubstrate;L,logs;P,PVCpipe;S,stones;SS, sandsubstrate;T,tree.

bark.Theindoorareaswereoff-viewcementcageswithadrinkingtroughandbath(total surfaceareaof10m2each)(Soriano,Ensenyat,Serrat,&Maté,2006).

DailyManagement

Themanagementprotocolallowsthebearstogointotheiroutdoorenclosuresaccording tothehoursofdaylight(between9:00a.m.and4:00p.m.inspring;9:00a.m.to8:00p.m. insummer;9:00a.m.to7:00p.m.inautumn).Thedietofferedwasseasonallyunvaried andconsistedof8kgoffruitandvegetables,4kgofmeat(amixtureofhorse,chickenand veal),2kgofdogchowand1kgofbreadonceadayforeachbear,providedintheindoor areasintheevening.Theold♀andtheyoung♀sleptseparatelyintheirrespectiveindoor enclosures.

Duringthestudyphase,theanimalstookpartinatwice-dailyenrichmentsession.Each bearreceivedthesameenrichmentdevicepersession.Duringthefirstsession,thekeeperput theenrichmentdeviceintheenclosurebeforetheanimalswereletintothespace,ataround 9:00a.m.Thesecondenrichmentdevicewaspreparedbythekeeperaround1:00p.m.and wasthrowninto theenclosure fromthe visitorviewingarea.The schedulefor different enrichmentdevicesforbothsessionsconsistedof31devices,twoofwhichwereusedeach dayofthemonth,followingthesamepatternduringallthemonthsofstudy.Inaddition, thereweredifferentkindsofenrichmentdevices;forexample,(1)feeding,whichprovided elementsthatcontainedfood,suchaslivefish[thefeedingoflivevertebratesisillegalin somecountries],vegetablesinsideasackorfruitinsidetrafficcones;(2)sensory,elements thatmaximizeolfactorycapabilities,suchasdifferentspicesorthefaecesofherbivores; and(3)occupational,itemsthatmaximizethephysicalandmanipulativecapabilities,such asballs,tyresortrafficcones(Soriano,2013).

These animals did not have any training programme that would facilitate veterinary practicesorbodymaintenance,suchasfootordentalcare.

AbnormalBehaviours

InFebruary2004,veterinaryexaminationofthesetwofemaleswascarriedouttodiscount physicaldiseaseasapotentialfactorinfluencingbehaviour.Thediagnosesestimatedthat theundesirablebehavioursobservedinthesebearswereconsideredabnormal.

Eachbeardemonstratedadifferent typeof abnormalbehaviour,on theonehand the old♀showedanoralabnormalbehaviourandontheotherhand,theyoung♀developeda locomotorstereotypy.Theold♀displayedepisodesofbitingatreetrunkthatwaspartof theenclosurefurniture.Thedescriptionofthisbehaviourwastheanimal,inafour-legged position,partlyintroduceditsmouthoverthe tree,andrepeatedlyopenedandclosedits mouth,tighteningits jawagainstthebaseofthe trunk.Thisbehaviour wasclassifiedas a‘state’, because it hadameaningful durationandit could betimed withastopwatch

(Fig.2A)(Lehner,1996).Theyoung♀demonstratedabehaviourthatwasrepetitiveand

ofshortduration,whichconsistedofabruptlyliftingtheheadupwardand/ortothesidein aswinging,oftencirculararc,ordippingtheheadtothegroundwithoutbreakingstride whilewalking.ThisactionhasbeendescribedinGiantpandasandwasnamed‘head-toss’

Fig.2.Diagramofabnormalbehavioursforbrownbears:A.Old_♀;B.Young_♀.

(Lindburgetal.,2003).Thisbehaviourwasclassifiedasan‘event’,definedasamomentary

behaviour(onlylasting5s)(Fig.2B)(Lehner,1996). DataCollection

ThestudyperiodwasfromMarchtoDecember2004.Theobservationsessionslasted one-hourand63hoursofobservationswererecordedusingamulti-focaland continuous-samplingmethod(Martin&Bateson,2007).Thestudiedvariablesincluded:

1. Seasonalperiods:21hoursofobservationwereconductedwithineachseason:spring (30 March–7 June 2004), summer (28 June–16 September 2004) and autumn (22 September–20December2004).

2. Abnormalbehaviours:fivedifferentaspectsofthisvariablewerestudiedineachsession: (1)percentageoftimeinvestedonabnormalbehaviour;(2)duration(sec),definedasthe amountoftimethebearengagedintheabnormalbehaviourandwasonlymeasuredfor theoldfemale’sepisodes;(3)intensity(sec),definedasthetimethatelapsedbetweentwo consecutiveabnormalstatesorevents;(4)occurrence,definedasthenumberofabnormal statesoreventsobservedduringeachsession;and(5)spaceusefrequency,definedas animalenclosurelocalizationmeanwhilethebearshowedtheabnormalbehaviours.The enclosurewasdividedintoeightsimilarlysizedzonesfromZone1toZone8(Fig.3). DataAnalysis

AlldataanalyseswerecalculatedusingtheStatisticalPackagefortheSocialSciences (SPSSInc.,Chicago,IL60606,USA)Version21.0forWindows.Normalitywasassessed usingKolmogorov–Smirnovtest.ArejectioncriterionofP<0.05wasappliedtoalltests. Therelationshipbetweenseasonalperiodsandtheduration,intensityandoccurrencewere obtained through the Kruskal–Wallis test (Lehner, 1996). Meanwhile, the relationship

Fig.3.Diagramoftheenclosureforbrownbearsshowingthedivisionoftheareasforthestudy ofspaceuse.

betweentheseasonalperiodsandtheuseofspacewereobtainedthroughchi-squaretest. Theadjustedresidualstatisticusedhadanabsolutevalueof1.96foranormaldistribution

(Haberman,1978).

Results

Forbothfemalesthe %oftimeinvestedonabnormalbehaviour washigherinspring followedbysummerandautumn(old♀;autumn:8.10%;spring:27.74%;summer:9.34%; young♀;autumn:7.50%;spring:11.75%;summer:9.12%).

Themeanandstandarddeviationoftheduration,intensityandoccurrenceofabnormal behaviourspersessionforthetwobrownbearfemalesareshowinTable2.Theabnormal behaviour duration was statistically significant higher inspring than insummer andin autumnforbothfemales.The intensityof abnormalbehaviour onlyshowed statistically significant difference for the young ♀. In thiscase, the intensity showed a statistically significanthighervalueduringautumnthaninsummerandinthespring.Theoccurrence ofabnormalbehavioursshowedstatisticallysignificantvaluesforbothfemales.Theold♀

showedahighervalueinautumnthaninsummerandinthespring.However,theyoung♀

showedahighervalueinspringthaninsummerandautumn(Table3).

Inrelationtospaceuse,theold♀alwaysdevelopedtheabnormalbehaviourintheZone 4whichfrequencywas54boutsinautumn,47boutsinspringand49boutsinsummer.

Table 2. Mean_±standarderrorofmean(SEM)fortheduration,intensityandoccurrenceof abnormalbehavioursforeachseasonalperiodandsessionintwoBrownbearUrsusarctosfemales:

nold_♀=137;nyoung_♀=4283(wheren=numberofobservedepisodesintheold_♀andeventsin theyoung_♀). Duration(sec) Mean_±SEM Intensity(sec) Mean_±SEM Occurrence(no.of abnormalbehaviours) Mean_±SEM OLD♀ Autumn 268.6±31.0 87.1±17.0 53.7±6.2 Spring 1081.7±111.3 207.1±37.8 2.1±0.3 Summer 391.4±61.9 299.5±58.8 2.8±0.5 YOUNG_♀ Autumn 290.6_±81.5 310.7_±66.3 1.9_±0.5 Spring 422.9_±35.9 41.2_±2.7 84.6_±7.2 Summer 328.3_±39.6 64.1_±12.5 65.7_±7.9

Table3. Kruskal–Wallisvaluesthatshowtheeffectofseasonalperiodontheduration,intensity andoccurrencefortwoBrownbears.

Duration(sec) Intensity(sec) Occurrence(no.of abnormalbehaviours)

H d.f. P H d.f. P H d.f. P

Old♀ 54.51 2 0.00** _{2.79 2 0.24 15.70 2 0.00}**

Young_♀ 733.02 2 0.00** _{810.59 2 0.00}** _{733.02 2 0.00}**

**_{StatisticallysignificantdifferencesP<0.05;H,Kruskal–Wallistest;d.f.,degreesoffreedom.}

Theyoung♀useofspaceshowedstatisticallysignificantdifferencesduringtheseasonal periods(X2=671.88;df=14;P=0.00**).Thisfemaleusemorefrequentlyzone6thanthe others. In autumn,thisfemaleshowed abnormalbehaviour withstatisticallydifferences more frequently inZones1, 2, 3, 4 and 5.In spring,the young ♀ developed abnormal behaviourwithstatisticallydifferencesmorefrequentlyinZones6and8.Insummer,this femaleshowedabnormalbehaviourwithstatisticallydifferencesmorefrequentlyinZones 6and7(Fig.4).

Discussion

Theabnormalbehavioursinthefemalesof thisstudyshowedindividualpatterns.The young ♀ showed a locomotor stereotypy also observedin otherstudies inbrown bears

(Spendrup &Larsson, 1997), Polar bears(Ames, 1993; Hare, 1995; Fernandez, 2010)

Fig.4.Frequencyofthespaceuseduringabnormalbehaviourforeachseasonalperiodinthe youngbrownbear.

behaviourswerealsoobservedinGiantPandas(Lindburgetal.,2003)andbrownbears

(Montaudouin&LePape,2005;Soriano,Vinyoles,&Maté,2016).

Onthe onehandandtakinginto account theunacceptable abnormalbehaviour value higher than10% described byBroom(1983),the unacceptable welfarevaluesfor both females of thisstudy would be observed inspring (old ♀: 27.74%; young ♀: 11.75%). However,thesevalueswouldbeacceptableinautumnandsummerforbothfemales.Onthe otherhand,MontaudouinandLePape(2005)encodedtheamountofstereotypyin:(1)no stereotypy;(2)low:lessthan21%oftime.Inthiscase,itwouldbeincludedthepercentages oftimeinvestedinabnormalbehaviourforbothfemalesinautumn(old♀:8.10%;young

♀:7.50%)andsummer(old♀:9.34%;young♀:9.12%)andonlythepercentageofyoung

♀inspring(11.75%);(3)medium:21%to45%oftime.Itwasonlyobservedfortheold

♀duringspring(27.74%);and4)highmorethan45%oftime.Itwasnotobservedinthis study.

Thestudy ofAmes(1993)inPolarbearsalsodescribedindividualpatterns of abnor-malbehavioursandalsoseasonalvariationsinthefourperiods–spring,summer,autumn andwinter–.Thisstudyincludedfivepolarbearmalesandeightpolarbearfemaleswhich showedsixdifferentkindsoflocomotorstereotypyonlandandinwater.Therewasa sub-stantialvariationintheamountofstereotypicbehaviourforthefemales,levelsrangedfrom 0%to59.9%andforthemalesrangedfrom0%to45%.Inthiscasethelowestpercentageof stereotypicbehaviourwaslowerthanbrownbearsofthisstudyandhighestlevelishigher, too.The durationof thesebehaviours rangedfrom 8secto50secand itwere different thanobservedinbrownbearsofthisstudythatrangedfrom5sec–fortheyoungfemale’s events–to1743sec –for the oldfemale’sbouts–.OnePolarbearmale andonefemale showedthelowestlevelofabnormalbehaviourinautumnandthehighestlevelinspring coincidingwiththeresultsofthisstudy.Moreover,onemaleandthreefemalesshowedthe lowestlevelofabnormal behaviourinautumnandthreemalesandtwofemales showed thehighestlevel ofabnormalbehaviourinspringlikethebrownbearsofthisstudy.The otherelevenPolarbearsshowedothervariationsoflowestandhighestlevelofstereotyped behaviour (winter-spring;spring-autumn; winter-summer;autumn-winter;spring-winter;

summer-winter;winter-autumn;summer-springand;autumn-summer,respectively).Polar bears may be are more susceptible to develop stereotypic behaviours than the rest of the bears because is more difficult to reproduce in captivity the extreme seasonal conditions.

CarlsteadandSeidensticker(1991)studiedstereotypicpacinginanAmericanblackbear

andobservedtwopeaksrelatedtomate-seekingbehaviourpredominatinginthelatespring andforagingbehaviourinthelatesummerandfall.Theseresultsarevery similartothe observedinthetwobrownbearsofthisstudy.Insummer,thebrownbearsofthisstudymay bearelesssusceptibletodevelopabnormalbehavioursbecausetheweatherconditionsare thesamethaninwildconditionsandthereisnotmatingorhibernationfeedingnecessities. In spite of the winter period was not observed in this study of brown bears, it is known that the winter sleeping isa species-typicalbehaviour. Therefore,more specific studiesare necessary todeterminethe role of hibernationin thewelfare of thesebears in zoological institutions. The hibernation period in bears is reliant on several differ-entfactors,including:(1)externalfactors,suchastemperatureandfood availability;(2) internalfactors,suchas hormonalchanges;and(3)acombinationof factors(1)and(2)

(Brown,2009;Möstl&Palme,2002;Stirling,1993;Ward&Kynaston,2003).The

zoo-logical institutions that house native species do not need to invest in large amount of money inair-conditionedor heatedenclosures becausethe localweather conditionsare the same. For example, at Ueno ZoologicalGardens, Japan, there is a Japanese black bear U. thibetanus japonicus enclosure that was designed to include an indoor enclo-surefor hibernation,inordertoencourage thisspecies-typicalbehaviour. Thisspecially designed denmakesit possibletostudy theanimals during hibernationandallows vis-itors toobserve the bearsevenduringthe winter-sleeping period(Itoh, Ide,Kojima, &

Terada,2010).Therearealsobearsinzoologicalinstitutionsthatcannothibernatebecause

theyarefarawayfromtheirnaturalenvironment,suchasthebearsatBarcelonaZoo.In thiscase,the welfareimplicationsof theinabilitytohibernateareunknown.Inorderto reproducethisparticularspecies-typicalbehaviourinaninstitution,itwouldbenecessary toadapt thehusbandry andmanagementprotocols, andthedesignof theenclosure and dens.

In relationtothespaceuse,theyoung ♀mightusemorefrequently thezone6 ofthe enclosurebecauseitistheplacemostplaneandmoreawayfromthevisitor’sarea.

The expressionof abnormal behaviours could be theresult of the conditions in zoo-logicalinstitutionsnotreproducingaccuratelytheconditionsinnature,whichpermitthe crepuscularbrownbearstoexperiencetwoseasonalpeaksinspecies-specificbehaviours (i.e.reproductioninspringandfoodstoreinautumn).Inordertoachievethesedesirable variationsandmeetindividualneeds,therearefactorsthatshouldbeconsideredandshould beincludedinthedailybear-managementprotocols(Soriano,2013).

1. Dietcomposition.Someformofseasonalvariationshouldbeincludedtoprovisionof diet, makingitmoresimilartothevariationsthat wouldbe experiencedinthewild. So,BrookfieldZoomanagersimplementedseasonaldietsforbrownbearssuccessfully becausethebearslostweightandaremoreactivewithlessaggressionandstereotypic behaviours(Watts,2009).Moreover,somestudiesthatappliedfeedingenvironmental

enrichmentinbrownbearsalsoreducedstereotypicbehaviours(Grandia,VanDijk,&

Koene,2001;Larsson&Tove,1995;Morimura&Ueno,1999).

2. Enrichmentprogrammes.Introduce seasonalvariationsintothe designandprovision ofvariousenrichmenttechniques;forexample,designanewenrichmentdevicewith salmoninsummerorintroducedriedfruitsinautumn(Hare,1995;Soriano,Vinyoles,

&Maté,2013).

3. Facilitydesign.Includeclimate-controlledfacilitiesanddenswithgrasses,moss,leaves, coniferneedles,andtreebranches(Brown,2009).Thereisalsoacrucialrelationship betweenthesizeandlayoutoftheenclosureandtheexpressionofabnormalbehaviours. Whenthefacilitiesprovidedarelargerandmorenatural,littleabnormalbehaviourare observedinbearsinzoological institutions (Seidensticker&Doherty,1996;Soriano

etal.,2006;Spendrup&Larsson,1997).

4. Socialconditions. Studiesshouldbecarried outtodeterminewhetherthe welfareof typically solitaryindividuals (as bears tendtobe innature) is worsewhen they are coexistingwithconspecificsthanwhentheyarehousedalone.Thisfactorcanbestudied throughbehavioural(i.e.expressionofabnormalbehaviours,theuseofspace,proximity) or/andphysiological(i.e.hormonalstudies) indicators(Kleiman,Thompson,&Baer, 2010).Itisimportanttotakeseasonintoaccountwheninstitutionsareparticipatingin breedingconservationprogrammes(Fa,Funk,&O’Connell,2011).

5. Effectofvisitors.Inzoologicalinstitutionsvisitorshaveaneffectontheexpressionof abnormalbehaviour.Thiseffecthasbeenclassifiedas:(1) positive,whenthevisitors decreaseabnormalbehavioursgenerally,andcanbeconsideredpartoftheenrichment programme(Claxton,2011;Robson,2004);(2)neutral,whenvisitorshavenoparticular effectonthe prevalenceof abnormal behaviours(O’Donovan,Hindle, McKeown,&

O’Donovan,1993;Sorianoetal.,2013);and3)negative,whenthevisitorsincreasethe

prevalenceofabnormalbehavioursordecreasethewelfareoftheanimals(Cunningham,

2005;Owen,2004;Sorianoetal.,2013).

6. Veterinarycare.Thehealthof allanimals inzoological institutionsshouldbe ahigh priorityasill healthor diseasemayaffectthe manifestationofabnormal behaviours. Protocols shouldincluding providingvaccines, ensuring anyinjuries or illnessesare cured, andmedication should be administered to avoidor treat parasite infestations

(Irwin,Stoner,&Cobaugh,2013).

7. Trainingprogrammes.Wherepossible,inordertofacilitateveterinarypractices,suchas administeringvaccinesorcollectingbiologicalsamples(e.g.blood,hair,urine,faeces), andbody maintenance(e.g.brushing hair or skin,filingnails or maintaining teeth), animals in zoological institutions should betrained topresent variousparts of their bodiesforveterinaryinspection(Ramirez,1999).

8. Transportation.Movinganimalsbetweeninstitutionsisalwaysstressful.Itisessential thatthewelfareoftheindividualshouldnotdiminisheitherduringoraftertransportation. Certainindividualfactorsshouldalsobetakenintoaccountbeforeanimalmovements; forexample,age,timespentincaptivity,healthandthemanagementguidelinesforthe species(Rees,2011).

Allthesefactorsinfluencethedevelopmentandmanifestationofabnormalbehaviours. Studyingeachaspectinmoredetailwouldbenecessaryifwearetoidentifytheoptimal

conditionsforthemaintenanceofbearsinthemostartificialenvironments(Swaisgood&

Shepherdson, 2005).Theultimate aimof thesekinds of studiesisthe reintroductionto

naturalhabitatsofbearsfromzoologicalinstitutions,asproposedbyVickeryandMason

(2003b),especiallybecausethesespeciesareatseriousthreatofextinctionintheirhome

territories.

Acknowledgements

WewishtothankSandraBalsandJuaniMelerofortheircollaborationonthisstudy.In addition,wewouldliketothankourfriendsEstherFernandezandMarcEscobarfortheir helpwritingthisarticle.WealsoappreciatetheEnglishrevisionbySudanshuKarandikar, ConchaSantolayaandSusannaFlavià.

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