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Behavioral persistence in captive : implications for reintroduction

Sophie S. Vickery' and J. Mason

Animal Behaviour Research Group, Department of Zoology, Oxford University, South Parks Road, OxfordOXI 3PS, UK

Abstract: We investigated the relationshipbetween stereotypic behavior and abnormalbehavioral persistence,a trait that could have potentiallynegative implicationsfor reintroductionefforts, for 18 Asiatic black bears ( thibetanus)and 11 Malayan sun bears (Helarctos malayanus)individually housed in a governmentconfiscation facility in Thailand.Reintroduction or augmentationprograms using captive-rearedanimals are typically less successful than those involving wild-reared con- specifics. One reason for this may lie in deficiencies in the behaviorof captive . Attributesof stereotypyperformance were quantifiedby observing bears from blinds. Mean stereotypyfrequencies ranged between 0 and 51% (mean = 18%, SE = ?3), of all observations,and stereotypyfrequency increasedwith age. To assess behavioralpersistence, 12 bears were trainedin a spatialdiscrimination task; once a performancecriterion had been met, furtherresponses were unrewardedand the ability to cease respondingwas assessed. The numberof trials for which bears continued respondingwithout rewardwas positively related to stereotypyfrequency. This finding suggests that captivity can exert subtle but potentiallydetrimental influences on behavioralcontrol that could possibly be manifesteven in non-stereotypic animals. In the wild, where behavior must be adaptive and flexible to meet fluctuatingconditions, such behavioral deficiencies could help account for reduced survivorshipof reintroducedsubjects.

Key words: Asiatic black , behavioral persistence, captive-bred, Helarctos malayanus, Malayan , reintroduction,stereotypy, Ursus thibetanus

Ursus14(1):35-43 (2003)

Given the current forecast for continued habitat conservationefforts will involve reintroduction, destruction and increasing species rates either to re-colonize areas after debilitatingfactors have (Wilson 1988), many animalpopulations seem destined been removed, or to augmentnumerically or genetically to decline, and the need for reintroductionas a conser- fragilepopulations. vation strategyis becomingincreasingly necessary. How- To date, release programs for bears have typically ever, the science of animal reintroductionis still in involved wild animals that have been kept in captivity its infancy, and failure rates are typically high (Griffith for only shortperiods of time, if at all (e.g. Jonkel et al. et al. 1989, Fischer and Lindenmayer2000). Four of 1980, Alt and Beecham 1984, Servheen et al. 1995, the world's 8 bear species are currently recognized Arquilliere 1998, Eastridgeand Clark 2001). However, as a facing high risk of extinction in the wild, in the for some bearpopulations it may not always be possible medium-termfuture (Hilton-Taylor2000). The survival to take wild animals for translocationwithout compro- of a fifth species, the Malayan sun bear, currentlylisted mising the fitness of the source population,and in these as datadeficient, is almostcertainly equally at risk, given situations,captive-bred individuals (which we define as the scale of habitat destruction throughout its range animalseither bor and raisedin captivity,or born in the with its coupled persecutionas a pest and capturefor the wild but raised in captivity from infancy), may be the pet andmedicine trades (Meijaard 1999). Forspecies with only alternative. sufficient remaining habitat, it is likely that future In addition to being more expensive and time-con- suming, reintroduction programs using captive-bred animals are almost universally less successful than those involving wild conspecifics (Griffithet al. 1989, email: [email protected] Frantzenet al. 2001, Clark et al. 2002). For example, 35 36 BEHAVIORALPERSISTENCE IN CAPTIVEBEARS * Vickery and Mason

Ginsberg (1994) reported that during the first year of discernible changes in behavior such as decreased be- release, the mortalityof captive-bredcanids was double havioral flexibility and reduced attention to the envi- that of translocatedwild animals.The poor survivorship ronment (e.g. Odberg 1978, Cronin et al. 1984). These of captive-bredanimals is often attributedto behavior- influences could be highly detrimentalto reintroduction al deficiencies (e.g. Kleimanet al. 1986), althoughhabi- efforts and importantly,because rearingconditions can tuationto humansmay also play a role (e.g. Buchalczyk cause such changes even without producing stereotypy 1980, Alt and Beecham 1984). The importanceof pre- (e.g. Jones et al. 1991), animals that do not stereotype serving species-typicalbehaviors, exposing potentialre- cannot be assumed to be unaffected. lease candidatesto complex environments,and providing Evidence has recently been presented of a correla- trainingfor particularskills is now well acknowledged tion between stereotypyand changes in the general or- (e.g. Kleimanet al. 1986, Beck et al. 1991, Griffinet al. ganization or control of behavior. Using bank 2000, Wallace 2000). However,reintroduction programs (Clethrionomysglareolus), Garer and Mason (2002) typically place less emphasis on the more general and found a correlationbetween stereotypyfrequency and an often subtle ways in which captivity can affect the be- individual's ability to suppressa learnedresponse when havior of animals, for example in terms of time allo- this response ceased to be rewarding (a measure of cation, activity levels, and behavioral flexibility (e.g. behavioral persistence). The most stereotypic animals Dittrich1984, Wemelsfelderet al. 2000, Swaisgood et al. were also more generally active and switched between 2001). different behaviors faster. Garer and Mason (2002) A particularlyconspicuous way in which animals argue that together, these correlationssuggest that cap- maintained in captivity often differ from their wild tivity can alter the organizationof behavior by acting counterpartsis in the performanceof stereotypies:seem- on the basal ganglia, the parts of the brain responsible Evidence ingly purposeless repeatedbehaviors that are invariant for selecting and ordering behavior patterns. in form (in that movements are the same on each was found for the same relationshipto exist in song- behavioral repetition)(Odberg 1978, Mason 1991a). The etiology (Gamer et al. In Press). Abnormal per- of these behavior patternsis not fully understood,but sistenceper se would undoubtedlybe a debilitatingtrait that animals rearing, husbandry,and genetic factors have all been for potentialreintroduction subjects, given flexible behavior to meet implicated (Mason 1993b). Individual factors such as in the wild must demonstrate further behavioraltemperament are also known to play a role irregularand unpredictablesituations. The impli- can behav- in stereotypydevelopment, because closely related ani- cation that time spent in captivity disrupt mals, rearedand housed under identical conditions, can ioral organizationat a fundamentallevel raises concern such as the vary in stereotypy frequency (Mason 1991b, Dallaire for other facets of reintroductionprograms, 1993, Mason 1993a). There are also markedspecies dif- trainingof complex species-typicalsurvival skills. to describe ferences in the form and prevalence of stereotypy that The aims of this study were two-fold: (1) and of be- appear to be related to a species' natural behavioral the forms, frequency, prevalence stereotypic Asiatic black bears and sun ecology (Morris 1964, Mason and Mendl 1997, Clubb havior in captive Malayan with and Mason 2001, Clubb 2002) and may reflect the bears;and (2) to test the hypothesis that, consistent of Garnerand Mason animals with degree to which the captive environmentrestricts that the findings (2002), levels of are more species' behavior.For example, across 23 species of car- higher stereotypy behaviorally per- nivore, Clubb and Mason (2001) found a positive cor- sistent. relationbetween a species' home range size in the wild and the frequencyof pacing in captivity. Bears are par- ticularly susceptible to the development of stereotypy, Methods and a propensity possibly related to their complex feeding Animals housing this were 29 bears: 18 Asiatic behaviorsand large home ranges in the wild, neitherof The subjects of study 11 and 11 sun which can be fully reproducedin captivity. Thus, even black bears (7 males, females) Malayan housed in a when maintainedin large naturalisticenclosures, bears bears (5 males, 6 females) individually gov- in Thailand.All animals were between often display stereotypy(e.g. Ormrod1992). ernmentfacility of been in the is a highly conspicuous behavior and it is 1.5 and 11 years age, having captured Stereotypy the Thai doubtfulthat animals exhibiting these aberrantbehavior wild shortly afterbirth and later confiscatedby Forest The holding facility was not patternswould be considered for release. However, its Royal Department. to the performance is sometimes associated with other less open public. Ursus 14(1):35-43 (2003) BEHAVIORALPERSISTENCE IN CAPTIVE BEARS * Vickery and Mason 37

Cages measured5 X 4 X 3 m (L X W X H), were con- Trials were conducted over 6 weeks between mid- crete floored, and had 3 walls of bars and 1 of cement, December 2000 and early February 2001. All bears leading to a covered den areaof 2 X 4 X 3 m. Apparatus received 1 session of 20 trials per day until a perfor- for climbing and tires and logs for enrichment were mance criterionof 90% (18 of 20 trials correct)over 3 providedin each cage, but no furtherenvironmental en- consecutive sessions was met. The probabilityof a bear richmentswere offered. Water was availablead libitum attainingthis criterionby chance is <0.0002 (binomial from 2 waternozzles locatedin the maincage section and distributionfor n = 20; P = 0.5). food was providedbetween 1500 and 1600 each day. Once the performance criterion had been met, sessions continued as previously but no rewards were Behavioral assessment given for responses to either apparatus.A criterionof Behavior was assessed by scan-sampling(i.e. observ- 65% or fewer responses made to the previously ing the behaviorof each bear in a pre-determinedorder, 'correct' apparatus(13 out of 20 trials or less) over 3 Martinand Bateson [1993:85]) from observationblinds consecutive sessions, was set to denote a return to between the cages. A scan of all bears took approxi- choosing between the two apparatus at random i.e. mately 13 minutes to complete, and approximately30 giving up or extinction(gradual waning of a conditioned scans were completed on each observation day. All response when the usual reinforcer is omitted, e.g. scans were evenly distributedbetween the hours of 0700 Mackintosh 1974) of the learned response. This was and 1800. Preliminaryobservations showed that bears our measure of the bears' ability to suppress and quickly habituated to an observer moving between modulate the previously rewardedbut now unsuccess- blinds, and in pilot studies, a significant correlation ful response. was found between behavior measured by the scan- ning methodand measurementstaken from video record- ings during periods of no disturbance,confirming that Measures and statistical analysis the observer's did not presence alterthe bears' behavior. Stereotypy frequency was calculated as a propor- Behavior was assessed from a total of 2,149 scans tion of all observations(the numberof observationsof made over 6 observationperiods (minimumobservation stereotypydivided by the total numberof observations). of 10 between June period days) 2000 and May 2002. To assess the relationshipbetween stereotypyfrequency Not all bears were assessed in each observationperiod; and responding during extinction trials, we used the 18 bears were studied or solely mainly from June 2000 level of stereotypymeasured immediately prior to task to February 2001, and the remaining 11 bears from presentation.For all other analyses, individual means October 2001 to 2002. May Seven mutually exclusive were calculatedacross all observationperiods to control of and categories posture locomotion were distinguished for possible seasonal effects (e.g. Carlsteadand Seiden- with 15 of normal along categories behavior (Vickery sticker 1991, Kolter and Zander 1997, Ames 2000). 2003) and 25 behaviorsor stereotypic elements (detailed Forms of stereotypy were categorized as being either in Table 1). behaviorswere definedas Stereotypic actions (1) locomotory (involving locomotory movements, e.g. that were and without repetitive, invariant, obvious pacing); (2) oral (involving movements of the tongue or and were >3 function, repeated times in succession. jaw area, e.g. sham chewing); or (3) other (movements falling outside of the previous categories, e.g. head Measurement of behavioral persistence swaying). To assess behavioral 12 bears persistence, (6 Asiatic The frequencies of the 3 types of stereotypy were black 6 bears, sun bears) were chosen at random and analyzed using non-parametricKruskal-Wallis tests be- taught a simple task discrimination (spatial cause the assumptionsof parametrictesting (homogeneity between 2 identical left and apparatus, right, that were of variance,normality, and linearity)were violated and to the bars of their clamped home cage). Each bear was could not be met throughtransformation. All other anal- rewardedfor on its pressing randomlyallocated correct yses werecarried out using GeneralLinear Models (GLM, lever. Rewardswere sections of fresh fruitor biscuit Minitab 12, Ryan and Joiner 2001). Differences in (C.P. Dog Food, Animal Pokphand Feed, Bangkok, stereotypy frequency due to a bear's species and sex Thailand)presented through a metal chute. Throughout were assessed using a model analogous to a 2-way all trials the experimenter was (SSV) positioned behind ANOVA, and the regression relationshipbetween time a black screen to minimize large unintentionalbody cues spent in captivity and was tested that stereotypy frequency might influence performance(Hediger 1981). using a model of the form:

Ursus 14(1):35-43 (2003) 38 BEHAVIORALPERSISTENCE INCAPTIVE BEARS * Vickeryand Mason

Table 1. Prevalence (number of bears of each species exhibiting behavior) and description of the stereotypic behaviors observed in 29 captive bears (18 Asiatic black bears and 11 Malayan sun bears) in Thailand, June 2000 to May 2002. Category Description Black bear Sun bear Locomotory Standardpace Locomotionalong a full cage length, body alignedwith the cage bars 5 10 or wall, head held centrally Standardweave Locomotionwith body perpendicularto cage bars or wall,front feet 4 2 occupy two or more positions,rear feet may be liftedand repositioned or only shuffled. Extendedpace As 'Standardpace' but pace exceeds one cage length 0 5 Loop Circularor ellipticalroute of locomotion 3 0 Head throw Throwinghead back and over shoulder. 3 0 Shortweave As 'Standardweave', but frontfeet occupy one definiteposition and may 0 1 hover over a second. Weave withsteps Standardor short weaving movementsinterspersed with back and forth 1 0 back and forth movements,body traces a T-shape. Steps 1 or 2 steps combinedwith 'Head sway'. 1 0 Turing movementsand elements used in conjunctionwith pace Head dip Muzzleangled down and moves towardcage floorat turn 1 9 Waterbath usage Waterbath stepped onto or sat on at turnof pace 2 8 Body rear Head and upperbody rearedat turnof pace, frontfeet liftedfrom ground 1 7 Head rear Muzzleangled up at turn,feet on ground. 0 1 Head scoop Head rearedand dippedin a single movementat turn,may be shaken at 0 1 the bottomof dip Body flop Head and upperbody rearedat turnand fall in a collapse-likemovement 0 1 Oralstereotypies Tongue flick Flickingtongue in and out of mouth 1 2 aroundmuzzle 0 1 Tongue curl Tongue curledup and O Jaw clamping Teeth clampedtogether repetitively. 0 1 Sham chewing Jaws moved as thoughfood is being chewed but the mouthis empty 0 1 1 Self-licking Repeated lickingof a body area, distinguishedfrom excessive groomingby 0 the invarianceand repetitionof movements 1 Retchingfood Food taken into the mouth,chewed, and retchedonto paw or surface, differs 0 fromregurgitation and re-ingestionin that food never reaches the stomach. Otherstereotypies 5 0 Head sway Body positionedin 'Shortweave' but primarymovement is a pendulum-like swayingof head witheyes directedat cage floor,front feet touch the ground at one definiteposition Head lean Head smoothlyleaned far back over shoulders,without throwing action 1 0 Head circle Head rotatedin a circularfashion. 1 0 a 0 1 Hopping Body positionedas in 'Shortweave' but weighttransferred between the frontfeet in hoppingmotion 0 1 Clawgrating Claws of frontfeet rasped togetherproducing a gratingnoise.

rewardedaffects the of extinction [e.g. Thompson Stereotypyfrequency speed et al. 1963]); (2) time in captivity(included as a covariate = time in captivity because a relationship between time in captivity and + species | sex covariate:time in captivity stereotypyfrequency was expected); (3) species; and (4) We hypothesized that bears displaying higher levels sex. The form of the model was: of stereotypy would take longer to extinguish respond- Stereotypyfrequency ing; this was tested using a similar model in which = taken to + trials to learn stereotypy frequency was log (natural)transformed to responses extinguish meet the assumptions of parametric testing. Other + time in captivity the model were: numberof trials factors included in (1) + species | sex covariates:responses taken to to reach the criterion(included as a cova- performance + trials to learn+ time in captivity riatebecause the numberof trialsfor which an animalis extinguish

Ursus 14(1):35-43 (2003) BEHAVIORALPERSISTENCE IN CAPTIVE BEARS * Vickeryand Mason 39

4 -

.

*

3 U a

. * 2

0r '..

c .

, U . 1,~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~? '"""'"" ' -100 -50 0 50 100 150 Partialledtrials to extinguish responding

Fig. 1. The relationship between stereotypy frequency (natural log transformed) in 12 captive bears (6 Asiatic black bears, 6 sun bears) and the number of unrewarded responses made during extinction sessions in Thailand, 2000 and 2001. Trials to extinguish responding are statistically controlled for: (1) the number of trials required to learn the initial discrimination; (2) time spent in captivity; (3) species; and (4) sex. The least stereotypic animal (bottom far left data point), although different from the other bears, is not statistically an outlier.

Results Relationship between response persistence Stereotypic behavior and stereotypy frequency A wide range of locomotory, oral, and other stereo- Bears made between 1 and 36 errors (mean= typies were observed. Pacing was the most prevalent 13 errors, SE = 3.07) before reaching the performance stereotypy, but other forms such as weaving, head criterion. No relationshipwas found between an indi- swaying, hopping, tongue flicking, and sham chewing vidual's learning rate and stereotypy frequency. The were also displayed (Table 1). Across all bears, numberof responsesmade by individualsduring extinc- locomotory stereotypies were significantly more fre- tion trials was highly variable,ranging between 11 and quent than either oral or other stereotypies (Kruskal- 115 (mean = 47 responses, SE = 8.6). As predicted,a Wallis H - 35.28, 2 df, P < 0.001). Frequencies of significant positive relationshipwas found between an locomotory stereotypy did not differ between the individual's stereotypy frequency and the number of species, but sun bears performedhigher frequencies of responses made during extinction (F = 4.41; 1, 5 df; oral stereotypiesthan black bears (H = 4.79, 1 df, P - R2 = 79%; 1-tailed P = 0.045; Fig. 1). In contrast,re- 0.029) and black bearsperformed greater frequencies of sponding in extinction was unrelatedto time spent in stereotypiescategorized as 'other' (H = 6.52, 1 df, P = captivity or a bear's species or sex. 0.011). Of the 29 bears assessed, only 2 (<7%) exhibited no stereotypic behavior. Individual mean frequencies of stereotypy ranged between 0 and 51% Discussion of all observations(n = 29; mean = 18%, SE = 3) and Few detailed studies of stereotypy in Asiatic black were unaffected by species or sex. Time spent in or Malayan sun bears are available for comparison, was to captivity found be significantly associated with but the forms and frequencies of stereotypy observed an individual's level of stereotypy, with older bears here were comparableto those reportedin zoo-housed = showing increasedfrequencies (F 7.59; 1, 23 df; R2 = bears of other species (e.g. Wechsler 1991, Ames 1994, P = 52%; 0.011). Kolter and Zander 1997, Langenhorst1998). Locomo-

Ursus 14(1):35-43 (2003) 40 BEHAVIORALPERSISTENCE INCAPTIVE BEARS * Vickeryand Mason tory stereotypieswere more common and performedat in a later study (Vickery 2003) no measure of food higher frequencies than non-locomotoryforms, a find- motivationpredicted the numberof responsesthat a bear ing consistent with that of Clubb and Mason (2001), made in extinction. The second alternativeexplanation who reportedcarnivores to be especially prone to pacing is thatanimals naturally differ in theirtendencies to form stereotypies.Interestingly, although frequencies of total routines (e.g. Benus et al. 1987, Mason 1991b) and our stereotypy did not differ between Asiatic black bears correlationis simply a product of these individual dif- and sun bears, significant differences were found in ferences. If this were the case, we might expect bears the frequency with which the 2 species exhibited oral that persist in the task to have the most habit-like, un- and other (non-locomotory,non-oral) stereotypies. Be- varying stereotypies but not to differ in their general cause rearing,husbandry, and housing conditions were activity levels or the rate at which they switch between virtually identical and bears of the 2 species did not behaviors. Work is on-going to investigate this; how- differin how long they had spent in captivity,these find- ever, in the meantime we believe that an effect of ings may reflect biological differences between the captivity on behavioral organizationis the most likely species. Previous studies have reportedthe development explanation. Interestingly, a bear's persistence in re- of differentforms of stereotypyin closely relatedanimal sponding was unrelatedto time spent in captivity, sug- groups (e.g. Wtirbelet al. 1996), and these might stem gesting that these represent 2 separate influences on from differencesin a species' naturalbehavioral ecology stereotypyfrequency. (e.g. Mason and Mendl 1997). Overall, if our hypothesis is correct, abnormal The finding that older animals, having spent more behavioralpersistence induced by captivity could help time in captivity, display higher frequencies of stereo- explain why captive-bredbears often fare poorly after typy has been previously reported in bank voles, reintroduction.Particularly during the early stages of American (Mustela vison), and domestic pigs release, behavioralflexibility could be criticalto survival (Cooper and Odberg 1991, Terlouw et al. 1991, Mason as animals adapt their currentbehavioral strategies to 1993a). meet the demands of the wild environment.Deficits in As predicted, our results also show that an individ- behavioralorganization may impair an animal's ability ual's frequencyof stereotypycorrelated with behavioral to select the most appropriateaction for a given situation persistence. This is consistent with Garer and Mason and to modify its immediatebehavior as environmental (2002) and supports the hypothesis that time spent in conditions change. Stereotypingbears are thus likely to captivity detrimentallyaffects behavioral organization. be particularlypoor candidatesfor release. However, the One reason that stereotypic bears are more persistent relationshipbetween stereotypy and behavioral persis- could be that dysfunction of the basal ganglia under- tence is unlikely to be a simple one, and it cannot be lies this behavioraldeficit, as was suggested by Gamer assumed that only animals visibly displaying stereoty- and Mason (2002). Disorders of this brain structure pies will be affected, because individuals differ greatly un- have previously been implicated in the performanceof in their susceptibilityto stereotypy for reasons yet stereotypiesinduced by stimulantdrugs (e.g., Lyon and explained. Furthermore,deficits in behavioral orga- Robbins 1975) and those associated with human nization can occur before the onset of stereotypy (see for stimulant-induced psychiatricdisorders such as autism (e.g. Turner1997) Cools 1980, Ridley et al. 1981 so even and schizophrenia (e.g. Ridley 1994). Furthermore, effects, and Jones et al. 1991 for rearingeffects), show low- captive stereotypic animals have been shown to have non-stereotypicbears may 'pre-stereotypy' altered basal ganglia functioning (e.g., studies assess- level changes in persistence. ing susceptibility to stimulant drugs, Terlouw et al. 1992). However, there are other possible explanations for the relationshipbetween stereotypyand persistence. Managementimplications behavioral The firstis thathighly stereotypicindividuals persist in the The possibility that captivity impairs researchis needed to task because they are hungrier; after all, stereotypy organizationsuggests that further to such detrimentalbe- frequencywas foundto peakprior to feedingtime, andthe elucidate the best ways prevent task was food-related. However, stereotypy frequency havioral changes. Reintroductionprograms are faced was not correlated with learning rate, as would be with balancingthe benefitsof time spent in captivity(for with the expected if highly stereotypic animals were more food rehabilitationor pre-releasetraining) potential of behavioral motivated (because motivation and learning are highly damage that captivity can exert in terms bears in naturalistic correlatedin operant studies e.g. Tarpy 1982:300), and deterioration.Maintaining large, Ursus 14(1):35-43 (2003) BEHAVIORALPERSISTENCE IN CAPTIVE BEARS * Vickeryand Mason 41 enclosures, in which they can perform a full range of Biological Sciences Research Council (BBSRC). G.J. naturalbehaviors and exert control over their environ- Mason was supported by a BBSRC David Philips ment, is likely to offer some protection against behav- ResearchFellowship. ioral deficits. Furthermore,environmental enrichment has had some success in reducing the development of stereotypies, particularlywhen introducedearly in life Literaturecited (e.g. Odberg 1987, Callard et al. 2000), a time when ALT, G.L., AND J.J. BEECHAM.1984. Reintroductionof animals seem most susceptibleto the detrimentaleffects orphanedblack bear cubs into the wild. WildlifeSociety of a restrictedenvironment (e.g. Sutanto et al. 1996). Bulletin 12:169-174. However, fully meeting the needs of bears in managed AMES, A. 1994. The welfare and management of bears in enclosures is a considerablechallenge, and Stiver et al. zoological gardens.Universities Federation for Animal Welfare Animal Welfare Research (1997) reported that American black bears (Ursus (U.F.A.W.) Report Number7. UniversitiesFederation for AnimalWelfare, americanus) reared in naturalisticenclosures still large PottersBar, UK. showed poor post-release survival. These authors con- . 2000. The managementand behaviourof captive cluded that it was to release inappropriate pen-reared polar bears. Dissertation,The Open University,Milton bears into the wild given the limitationsof presentman- Keynes,UK. agement methods. In view of problems experienced ARQUILLIERE,A. 1998. Experimentalreintroduction of brown when releasing first generation captive-bred animals, bearsin the FrenchPyrenees. Oryx 32:8-10. a better alternativemight be to introduce captive-bred BECK, B.B., D.G. KLEIMAN,J.M. DIETZ, I. CASTRO, C. bears to controlled areas of wild or semi-wild habitat CARVALHO,A. MARTINS,AND B. RETTBERG-BECK.1991. (e.g. islands) and use their offspring for translocation Losses and reproductionin the reintroducedgolden tamarins projects. These cubs, having themselves been exposed Leontopithecusrosalia. Dodo 27:50-61. BENUS, R.F., J.M. AND G.A. VAN OORTMERSSEN. to natural conditions during their critical development KOOLHAAS, 1987. Individualdifferences in behaviouralreaction to a period, should have chances of survival comparable environmentin mice and rats. Behaviour100: to the of wild animals. changing offspring Similar methods have 105-22. been in reintroduction employed programs involving BUCHALCZYK,T. 1980. The in Poland.International other et al. Moore and Smith species (Beck 1991, 1991) Conferenceon BearResearch and Management 4:229-232. and have shown results. encouraging CALLARD,M.D., S.N. BURSTEN,AND E.O. PRICE.2000. Repeti- Although it may be some time before the reintro- tive backflipping behaviour in captive roof rats (Rattus duction of captive-bredbears is a necessary conserva- rattus) and the effects of cage enrichment.Animal Welfare tion measure,research is needed now to develop rearing 9:139-152. and management strategies which least compromise CARLSTEAD,K., ANDJ. SEIDENSTICKER.1991. Seasonal variation an animal's behavioral organization and enhance its in stereotypic pacing in an , Ursus chances of survival in the wild. Research efforts could americanus.Behavioural Processes 25:155-161. CLARK,J.D., D. HUBER,AND C. SERVHEEN.2002. Bear re- concentrateon the more common bear species such as introductions:lessons and challenges. Ursus 13:335-346. the American black bear, of which large numbers are CLUBB, R. 2002. The roles of foraging niche, rearing brought into captivity each year as orphanedcubs. In conditions and currenthusbandry on the development of this way strategiescould be developed for later use on stereotypiesin .Dissertation, Oxford University, the more vulnerable species, with which we cannot Oxford, UK. afford to make mistakes. , ANDG.J. MASON.2001. Are some species predisposedto develop stereotypybecause of theirforaging strategy in the wild? Pages 139-141 in V.J. Hare, K.E. Acknowledgments Worley, and K. Myers, editors. Proceedings of the Fourth We thank the Thai Royal Forest Department for InternationalConference on EnvironmentalEnrichment. The allowing us to studybears housed in theirfacilities, and in Shape of Enrichment,San Diego, USA. COOLS,A.R. 1980. Role of neostriatal particularP. Sanpote, Chief of Banglamung Wildlife dopaminergicactivity in sequencingand selecting behavioural facilitation Breeding Stationfor his supportthroughout this project. strategies: of processes involved in the best in a We arealso gratefulto threereviewers for theircomments selecting strategy stressful situation.Behavioural Brain Research 1:361-378. during the preparationof this manuscript. The work COOPER,J.J., ANDF.O. ODBERG.1991. The emancipation of ste- covered in this paper is from Ph.D. researchcarried out reotypieswith age. Page 142 in M.C. Appleby, R.I. Howell, by S.S. and the Vickery supportedby Biotechnology and S.C. Petherick, and S.M. Rutter, editors. 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