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Behavioral persistence in captive bears: a response to Criswell and Galbreath

Sophie S. Vickery' and Georgia J. Mason2 behavior [Odberg 1978, Mason 1991]) of captive can have detrimental correlates. They have AnimalBehaviour Research Group, been associated with reduced behavioral diversity Departmentof , OxfordUniversity, (Stolba et al. 1983, Shepherdsonet al. 1993, Swaisgood South Parks Road, OxfordOX1 3PS, UK et al. 2001), decreasedresponsiveness to environmental stimuli (Fentress 1977, Ormrod 1992, Langenhorst Ursus 16(2):274-279 (2005) 1998, Clubb 2001), reducedexploratory behavior (Lien and Klopfer 1978), poor maternalcompetence (Mason et al. 1995), injuryand reduced body condition(Sambraus 1985, Fraser and Broom 1990, Moon-Fanelli and This paper responds to criticisms raised by Criswell Dodman 1998), and reduced reproductive success and Galbreath(2005) regardinganalyses we used in an (Shepherdson 1994). Comparedto their non-stereotyp- earlierpaper (Vickery and Mason 2003), and shows that ic counterparts, stereotypic animals may also have their criticisms are unfounded. However, first, we altered neurochemistry, for example showing alter- present some backgroundto the original work. Vickery ations in dopamine (Dantzer 1986), serotonin (Vande- and Mason (2003), written toward the end of a long- broek et al. 1995), and opioid (Zanella et al. 1996, term study of captive bears, was timed to allow for Zanella and Mason 1997) functioning. Furthermore, presentationin 2002. One of us (SSV) was based at recent work on bank voles (Clethrionomysglareolus), Banglamung Wildlife Breeding Station in Chonburi mice (Mus musculus), (Amazona amazonica), province, Thailand, a sanctuary which individually and 2 species of songbird (Parus caeruleus and P. housed Asiatic black bears (Ursus thibetanus) and palustris) and rhesus monkeys (Macaca mulatta) has Malayan sun bears (Helarctos malayanus) in virtually shown that stereotypic animals are more 'persevera- identical conditions, providing a unique opportunityto tive', i.e. more behaviorally persistent than are their investigatebears' behavioralresponses to . The less stereotypic conspecifics (Gamer 1999, Garnerand behaviorof 29 bears was observed over 2.5 years. This Mason 2002, Gamer et al. 2003a,b, Lutz et al. 2004, was the total numberof individualsavailable for study, Latham 2005). Our aim was to test for a similar barring those that were sick or whose records were correlation in bears, to investigate the generality of incomplete. Of these, 21 were put through learning these findings. For species such as these, such an tasks to test the hypothesis that their effect could also have conservation implications, stemmed from a general inability to switch behaviors potentially helping to explain the low reintroduction appropriately.These learning tasks were time-consum- success currentlydisplayed by captive-bredanimals. In ing to run, and thus it was not possible to test all 29 reintroductionprograms, captive-bred animals general- bears. Twelve bears were tested in Year 1 (the data ly fare far worse than translocatedwild conspecifics presentedin Vickery and Mason [2003]), and a further9 (Griffith et al. 1989, Ginsberg 1994, Frantzen et al. bears in Year 2. Both years' data are presented in 2001), and this certainly seems true for bears (Alt and Vickery and Mason (2005). In addition, the properties Beecham 1984, Stiver et al. 1997, Eastridgeand Clark of all 29 bears' stereotypieswere analyzed for effects of 2001, Clark et al. 2002). For example, Stiver et al. time in captivity, sex, and species (presentedbriefly in (1997) reportedthat of 23 pen-rearedAmerican black Vickery and Mason [2003], and more fully in Vickery bears (Ursus americanus) released in east Tennessee and Mason [2004]). between 1982 and 1995, 6 were known to die, 5 It is well recognized that the stereotypies(repetitive, caused nuisance problems, and 2 were killed illegally invariantand seemingly functionlessforms of abnormal by humans. The 2 main findingspresented in Vickery and Mason (2003) were: (1) a positive correlation between an 1Presentaddress: Welfare Division, Department for individual's stereotypy frequency and the number of Environment,Food and Rural, Affairs, 1A Page Street, trials for which it continuedto respond without reward LondonSW1P 4PQ,UK; [email protected] (a measureof behavioralpersistence), and (2) a positive 2Presentaddress: Centre for the Studyof AnimalWelfare, correlationbetween stereotypyfrequency and time spent Departmentof Animal and PoultryScience, Universityof we divide Criswell and Galbreath's Guelph,Ontario N1G 2W1, Canada;[email protected] in captivity. Here,

274 BEHAVIORALPERSISTENCE: RESPONSE 275 criticisms of our work into 2 categories:those aimed at Statistical analyses our general scientific approach,and those aimed at our We categorize Criswell and Galbreath's statistical specific statisticalanalysis. criticisms into those that are wrong and those that are right but unimportant.First, we deal with issues about which they are simply wrong. Criswell and Galbreath Our aims and suggest that we would have obtaineda betterfit had we general chosen In S' (mean stereotypylevels across up to 6 ob- scientific approach servationperiods between June 2000 and May 2002) in we and did we use Why did do this work, why the place of In S (stereotypy levels measured immediately we did? One of Criswell and Galbreath'swor- subjects prior to task presentation).Although we appreciatethe ries is that "It was never made clear ... 29 bears why" suggestion, this is irrelevantbecause these 2 stereotypy were used in one and 12 in another.The analysis impli- measures are far from interchangeable.Levels of ste- cation is that we selected a non-random subset of reotypy can vary with season, time in captivity,environ- animals from which it would be to clearly illegitimate mentalchange andother factors, and an individual'slevel further. However, we did no such extrapolate thing. of responding might also vary over time This was an in which we opportunisticstudy simply (Garner1999, Garneret al. 2003a). Thus, when inves- used all the animals that were available to us and tigatinga relationshipbetween stereotypyand extinction, collected as much data as possible within logistic it is sensible to measure these 2 variables as closely constraints. For example, we ran the learning experi- togetheras possible. The measureof stereotypydenoted ments over 2 years because so few bears could be S was used in our extinction analysis (Criswell and investigated simultaneously. Galbreath[2005] Eq. 1) because this was taken imme- Second, Criswell and Galbreath claim that we diately priorto task presentation.However, for the same "lumped all the bears available" into a single treatment reason - because an individual's stereotypyfrequency group, thereby foregoing the opportunity to study a might differover the courseof a year- when looking for control group of bears. However, in fact, there was a relationshipbetween averagestereotypy frequency and no appropriatecontrol group, because all the bears that the number of years spent in captivity, it is most could be studied (i.e. those that were single-housed) appropriateto assess on several were housed in near-identicalcages and all except 2 stereotypy frequency occasions the and calculate an overall exhibited stereotypy. It was for this reason that our throughout year mean. Thus the measure used in our 'time in study was correlational. Third, they claim that our captivity' and Galbreath S', "... inference would have been strongerhad [we] used analysis (Criswell [2005] Eq. 2), a mean of measured an experimentaldesign in which those bears that had represents stereotypy frequencies over to 6 observation previously been removed from enriched enclosures to up periods. claim that it would be small cages were compared to bears lucky enough to Second, they impossible to datasets remain behind in the enclosures." Here, we emphasize properlylog-transform containingzeros. In fact, this is that we did not move the animals; ratherour subjects problem commonly solved in practiceby adding 1 to were bears that had been housed in cages long before each value prior to transformation(Martin and we arrived. Bateson 1993:151). Finally, they incorrectly imply that we condemn We now respond to statistical critiques that are reintroductionas a conservationtool. For example, they technically correct but are ultimately unimportantfor assert, "These findingslead Vickery and Mason, in turn, inference in this study. Criswell and Galbreath(2005) to question the potential success of reintroduction first claim that we reversedthe "directionof causality". programs with bears held captive for substantialtime Our use of stereotypy as the dependent variable was periods". In fact, there was alreadyample evidence that appropriatebecause we were suggesting stereotypy to reintroductionprograms involving captive-bred bears, be a productof underlyingchanges that increasegeneral and indeed captive-bredanimals of a range of species, behavioralpersistence (see also Garnerand Mason 2002). are less successful than those involving their wild However, as Criswell and Galbreath(2005) point out conspecifics. Our paper simply sought to raise and test themselves, "in a correlationalstudy, that switch is not so ideas that might explain why this is so, with the aim of serious." Our study was indeed exactly that-a correla- helping biologists improve reintroduction success in tional study, seeking to determine if 2 phenomenaco- the future. varied. Furthermore,while they are correct that for the

Ursus 16(2):274-279 (2005) 276 BEHAVIORALPERSISTENCE: RESPONSE

firstyear's dataalone (n = 12), if extinctionis takenas the final model retains only those variables that have dependent variable the relationship with stereotypy predictivepower-this will result in a final model that becomes non-significant,if we repeat this analysis for is, as a whole, significant (as was true for the reduced the full dataset (n = 21; see Vickery and Mason 2005), 'best subsets' model above: P = 0.017). However, if swapping stereotypyand extinction in the model makes a variableis expected to have an effect on the dependent no differenceto the significanceof the effect (stereotypy variable(for example, in this case, time in captivitywas as dependent variable-our preferred, for reasons of known to have an effect on stereotypy frequency), it logic: F= 5.49; 1, 13 df; 1-tailedP = 0.018; extinction should be included in the model even if it is non- respondingas dependentvariable: F = 5.49; 1, 13 df; 1- significant,to act as a blocking factor (Grafenand Hails tailed P = 0.018). Thus with a larger sample size the 2002). If non-significantvariables are included in this relationship holds regardless of whether stereotypy is way, the model as a whole may well be non-significant, deemed a dependentor independentvariable. but that does not invalidateany significantrelationships Second, was our model "over-fitted"?Criswell and that arise from it, which remain true and significant Galbreath(2005) claim that one of our models (their effects (Grafen and Hails 2002; F. Marriott, Oxford Eq. 1, which examinesthe relationshipbetween stereotypy University Statistics Department,Oxford, UK, personal and behavioral persistence) included too many terms, communication,2003). leaving us with few remainingdegrees of freedom. We Fourth and finally, did we use models from entirely counterthat it would have simply been illogical to have the wrong statistical family? Criswell and Galbreath ignored the variables incorporated here-they were criticize us for using parametricmethods on bounded included to control for potential confounds, i.e. other data:our stereotypydata were expressed as proportions factorsknown to affect stereotypyor extinctionlearning of time, and thus logically could not be greater than (see below). For instance, although Criswell and 1 or less than 0. This makes them, strictly speaking, Galbreath(2005) claim there were "complex interac- binomial. However, like many behavioral data, in tions", in fact we includedonly one: species x sex, which practice they (or rathertheir residuals from the model) they acknowledgehas an importanteffect on stereotypy were not in fact significantly different from normal. (see their Fig. 1). Many statisticianstake the view that (This is because, while theoreticallybounded, in practice a model shouldpartition out as muchvariance as possible very few animals performedzero stereotypy, while - (Grafenand Hails 2002, Kaps and Lamberson2004), just unsurprisingly-no animals spent 100% of their time as we did. Furthermore,if, for the sake of argument,we stereotyping; thus even the raw data approximated pare down the model using Minitab's best subsets normality). Furthermore,GLM's assumptions of ho- regression command (which examines all possible mogenous variance were not violated, contrary to regression models and identifies the model that gives Criswell and Galbreath's claims. Data transformation the largest R2 value; Minitab 12.0, Ryan and Joiner is a commonly used and widely accepted method of 2001), the best fitting model excludes the interaction correcting for non-normal distribution (Martin and term that Criswell and Galbreathare concerned about Bateson 1993:150, Grafenand Hails 2002). Proportional and leaves only time in captivity and extinction as the data are commonly transformed using the angular 2 most importantexplanatory variables. Importantly, in (arcsine-square)transformation (Martin and Bateson this model, the relationship between extinction and 1993:150), but the appropriatenessof any transforma- stereotypyholds (F = 3.99; 1, 9 df; 1-tailedP = 0.039). tion always needs to be checked beforehand(Tabach- Finally, running our original (full) model on the nick and Fidell 1989, Grafen and Hails 2002). In the complete dataset, with its greater degrees of freedom, case of the Year 1 data reportedin Vickery and Mason gave us the same results (Vickery and Mason 2005). (2003), the angular transformationactually resulted in Thirdly, Criswell and Galbreath(2005) state that we non-homogeneous variance, and a logarithmic trans- "failed, however, to reportthat their model as a whole formationinstead proved most appropriate.In contrast, fails to significantly explain variation in stereotypy no transformationwas needed for the 'time in captivity' were frequency." While true, this is a red herring: this is analysis. For both of these analyses, the residuals simply irrelevantto the hypothesis under test. Whether normally distributed, thus confirming multivariate a model is significantoverall depends on whethernon- normality, that is, that each variable and all linear significant variables within the model are omitted, or combinationsof the variableswere normallydistributed instead retained(as in our work). In a predictivemodel, (Tabachnick and Fidell 1989:70). Figures 1 and 2 non-significantvariables are generally excluded so the present histograms and Anderson-Darling normality

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BEHAVIORAL PERSISTENCE: RESPONSE 277

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------*1*-** ---* ------I .05 ' .01 1 1 .01 .001 . * - .001 I I I -0.2 -0.1 0.0 0.1 0.2 -0.5 0.0 0.5 Residuals Residuals Average: 0.0000000 Anderson-Darling NormalityTest StDev: 0.0977666 A-Squared: 0.363 Average: 0.0000000 Anderson-Darling Normality Test N: 29 P-Value: 0.419 StDev: 0.316752 ASquared: 0.237 N: 12 P-Value: 0.727 Fig. 2. Tests for normality of the residuals from Fig. 1. Tests for normality of the residuals from the the GLManalysis testing for a relationship between GLM analysis testing for a relationship between stereotypy frequency and time in captivity (Equation stereotypy frequency and responding in extinction 2; n = 29): (a) histogram of residuals; (b) normality (Equation 1; n = 12): (a) histogram of residuals; (b) plot and Anderson-Darling NormalityTest. normality plot and Anderson-Darling NormalityTest. between extinction and stereotypy that was even plots and test statisticsof the residualsfor the extinction stronger than our original finding (Criswell and and time in captivity analyses respectively.Ryan-Joiner Galbreath2005:Table 3), but which they claimed to be and Kolmogorov-Smimov normality tests also verified "biologically uninteresting."They then acknowledge that the residualsconformed to the normal distribution. problems with their own model's assumptions in the Given that none of the assumptionsfor using general form of over-dispersion.This strikes us as unnecessary linear models was actually breached, it was perfectly effort when our original model was perfectly legitimate. appropriate to use them (indeed, regressions and ANOVAs are commonly used on time budget data for just this reason; Martin and Bateson 1993), and it is Conclusion unnecessary to insist on an alternative. Criswell and The findings we presented in Vickery and Mason Galbreath'sinitial alternativeresulted in a relationship (2003) were neither controversial nor unprecedented.

Ursus 16(2):274-279 (2005) 278 BEHAVIORALPERSISTENCE: RESPONSE

We found a strong relationshipbetween stereotypyand Literaturecited length of time in captivity (a factorcorrelating with bear ALT, G.L., AND J.J. BEECHAM.1984. Reintroduction of age). This positive correlationwas consistent with that orphanedblack bear cubs into the wild. Wildlife Society found in other species, such as pigs (Croninand Wiep- Bulletin12:169-174. kema 1984), mink (Mason 1993), mice (Wiirbel et al. CLARK,J.D., D. HUBER,AND C. SERVHEEN.2002. Bear 1996) and dogs (Siwak et al. 2001). We also found reintroductions:lessons and challenges. Ursus 13:335-346. R. 2001. The roles of a positive relationshipbetween stereotypy and behav- CLUBB, foraging niche, rearing conditionsand current on the of ioral persistence,just as we had predicted.Interestingly, husbandry development in carnivores. Dissertation, of to date this relationship has been found in all other stereotypies University Oxford,Oxford, UK. species in which it has been investigated(Gamer 1999; CRISWELL,A.R., AND GALBREATH,G.J. 2005. Behavioral Garnerand Mason Garer et al. 2003a,b; Latham 2002; in bears: a Ursus 16:268-273. as to whether such persistence captive critique. 2005), raising pressing questions CRONIN,G.M., ANDP.R. WIEPKEMA.1984. An analysis of effects reflect and Mason dysfunction (e.g. Vickery stereotyped behaviour in tethered sows. Annales de 2003). Furthermore,our concluding suggestions should RecherchesVeterinaires 15:263-270. of not have been controversial. The reintroduction DANTZER,R. 1986. Behavioral, physiological and functional captive-bredanimals often fails, and it is importantto aspects of stereotypedbehavior: review and a re-interpre- understandwhy. We made no claims to have discovered tation. Journalof Animal Science 62:1776-1786. the answer;we merely suggested a new, plausible, and EASTRIDGE,R., ANDJ.D. CLARK.2001. Evaluation of 2 soft- testable hypothesis. We are thus glad that Criswell and release techniques to reintroduce black bears. Wildlife Galbreathagree with our suggestion thatbears housed in Society Bulletin 29:1163-1174. more natural, enriched environments might differ in FENTRESS,J.C. 1977. The tonic hypothesis and the patterning New York of Science theirbehavior from the individuallycaged bears that we of behavior.Annals of the Academy 290:370-395. tested (though their phrase 'learning adaptation' sug- FRANTZEN,M.A.J., J.W.H. FERGUSON,AND M.S. DE VILLIERS. some misunderstandinghere; the effect is clearly gests 2001. The conservationrole of African wild dogs with As our captive not to do learningper se). paper suggests, Conservation100:253-260. bears in naturalisticenclosures, in (Lycaonpictus). Biological "Maintaining large, FRASER,A.F., ANDD.M. BROOM.1990. Farmanimal behaviour of naturalbehaviors which they can performa full range andwelfare. Bailliere Tindall, London, UK. their is to and exert control over environment, likely GARNER,J.P. 1999. The aetiology of stereotypy in caged offer some protection against behavioral deficits." animals. Dissertation,University of Oxford, Oxford, UK. Testing this hypothesis in the future would be both , ANDG.J. MASON.2002. Evidence for a relationship fascinatingand important. between cage stereotypies and behavioural disinhibition Given all this, we found Criswell and Galbreath's in laboratoryrodents. Behavioural Brain Research 136: criticismsof our paperto be a puzzling over-reaction.As 83-92. route- we have shown, our analyses, findings and conclusions , AND R. SMITH.2003a. Stereotypic correlateswith are not overturned by any of their criticisms. The tracingin experimentallycaged songbirds AnimalBehaviour 66: manner in which these criticisms are presented also generalbehavioural disinhibition. 711-727. distressinglymisses the key point: the reintroductionof , C.L. MEEHAN,AND J.A. MENCH.2003b. Stereotypies captive bears is prone to failure and it is vital that in parrots,schizophrenia and autism:evidence for seek to understand why. Our real misde- caged biologists a common mechanism. Behavioural Brain Research meanors, such as they are, appear merely to be (1) 145(1-2):125-134. from an n of 12, instead of publishing results just GINSBERG,J.R. 1994., reintroduction and the data were waiting until all our experimental processed conservation of canids. Pages 365-383 in P.J.S. Olney, of (Vickery and Mason 2005), and (2) remindingreaders G.M. Mace, and A.T.C. Feistner, editors. Creative an uncomfortabletruth: the very real currentfallibility conservation:interactive management of wild andcaptive of reintroductionattempts. animals. Chapmanand Hall, London, UK. GRAFEN,A., ANDR. HAILS.2002. Moder statisticsfor the life Acknowledgments sciences. Oxford University Press, New York, New York, Our thanks to Drs. J. Garner, S. Held, F. Marriott, USA. C. REED.1989. and J. Newman for discussion and statistical GRIFFITH,B., J.M. SCOTT,J.W. CARPENTER,AND conservation tool: status and advice, and to 2 anonymous referees for helpful Translocationas a species comments. strategy.Science 245:477-480. Ursus 16(2):274-279 (2005) BEHAVIORALPERSISTENCE: RESPONSE 279

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